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Parasitology Research

, Volume 117, Issue 7, pp 2139–2148 | Cite as

Skin mites in mice (Mus musculus): high prevalence of Myobia sp. (Acari, Arachnida) in Robertsonian mice

  • Natalia SastreEmail author
  • Oriol Calvete
  • Jessica Martínez-Vargas
  • Nuria Medarde
  • Joaquim Casellas
  • Laura Altet
  • Armand Sánchez
  • Olga Francino
  • Jacint Ventura
Original Paper

Abstract

Myobia sp. and Demodex sp. are two skin mites that infest mice, particularly immunodeficient or transgenic lab mice. In the present study, wild house mice from five localities from the Barcelona Roberstonian system were analysed in order to detect skin mites and compare their prevalence between standard (2n = 40) and Robertsonian mice (2n > 40). We found and identified skin mites through real-time qPCR by comparing sequences from the mitochondrial 16S rRNA and the nuclear 18S rRNA genes since no sequences are available so far using the mitochondrial gene. Fourteen positive samples were identified as Myobia musculi except for a deletion of 296 bp out to 465 bp sequenced, and one sample was identified as Demodex canis. Sampling one body site, the mite prevalence in standard and Robertsonian mice was 0 and 26%, respectively. The malfunction of the immune system elicits an overgrowth of skin mites and consequently leads to diseases such as canine demodicosis in dogs or rosacea in humans. In immunosuppressed mice, the probability of developing demodicosis is higher than in healthy mice. Since six murine toll-like receptors (TLRs) are located in four chromosomes affected by Robertsonian fusions, we cannot dismiss that differences in mite prevalence could be the consequence of the interruption of TLR function. Although ecological and/or morphological factors cannot be disregarded to explain differences in mite prevalence, the detection of translocation breakpoints in TLR genes or the analysis of TLR gene expression are needed to elucidate how Robertsonian fusions affect the immune system in mice.

Keywords

Skin mites Myobia Demodex Robertsonian fusions Mouse Prevalence 

Notes

Funding information

Field work and karyotyping of the mice from the Barcelona Robertsonian system used in this study was funded by the Spanish Ministerio de Ciencia y Tecnología (project number CGL2007-62111 to JV) and Ministerio de Economía y Competitividad (project reference CGL2010-15243 to JV). Financial support for genetic analysis was provided by the “Servei Veterinari de Genètica Molecular” (SVGM).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics statement

Permission to capture was granted by the Departament de Medi Ambient of the Generalitat de Catalunya (Spain). Animals were handled in compliance with guidelines approved by the Comissió d’Ètica en l’Experimentació Animal i Humana (CEEAH) of the Universitat Autònoma de Barcelona and by the Department d’Agricultura, Ramaderia, Pesca, Alimentació i Medi Natural (Direcció General de Medi Natural i Biodiversitat) of the Generalitat de Catalunya (reference of the experimental procedure authorization: DAAM 6328).

Supplementary material

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Supplemental Table 1 (XLSX 13 kb)
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Supplemental Table 2 (XLSX 10 kb)
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Supplemental Table 3 (XLSX 11 kb)
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Supplemental File 1

Sampling regions (Rb = Robertsonian translocated group; St = standard group) (PNG 3.03 mb)

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High resolution image (TIF 2091 kb)
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Supplemental File 2

16S rDNA fragment alignments (PNG 2.45 mb)

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High resolution image (TIF 16345 kb)
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Supplemental File 3

18S rDNA fragment alignments (PNG 2.88 mb)

436_2018_5901_MOESM6_ESM.tif (22.4 mb)
High resolution image (TIF 22938 kb)

References

  1. Akilov OE, Mumcuoglu KY (2004) Immune response in demodicosis. J Eur Acad Dermatol Venereol 18:440–444.  https://doi.org/10.1111/j.1468-3083.2004.00964.x CrossRefPubMedGoogle Scholar
  2. Baker DG (1998) Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin Microbiol Rev 11:231–266PubMedPubMedCentralGoogle Scholar
  3. Bochkov AV (2001) Parallel evolution of Myobiidae (Acari: Prostigmata) mites and jerboas (Rodentia: Dipodoidea). Parazitologiia 35:9–18PubMedGoogle Scholar
  4. Capilla L, Medarde N, Alemany-Schmidt A, Oliver-Bonet M, Ventura J, Ruiz-Herrera A (2014) Genetic recombination variation in wild Robertsonian mice: on the role of chromosomal fusions and Prdm9 allelic background. Proc R Soc B Biol Sci 281:20140297.  https://doi.org/10.1098/rspb.2014.0297 CrossRefGoogle Scholar
  5. Carty AJ (2008) Opportunistic infections of mice and rats: Jacoby and Lindsey revisited. ILAR J 49:272–276CrossRefPubMedGoogle Scholar
  6. Cruickshank RH (2002) Molecular markers for the phylogenetics of mites and ticks. Syst Appl Acarol 7:3–14CrossRefGoogle Scholar
  7. Dawson DV, Whitmore SP, Bresnahan JF (1986) Genetic control of susceptibility to mite-associated ulcerative dermatitis. Lab Anim Sci 36:262–267PubMedGoogle Scholar
  8. Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485.  https://doi.org/10.1534/genetics.107.071399 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Erbaǧci Z, Özgöztaşi O (1998) The significance of Demodex folliculorum density in rosacea. Int J Dermatol 37:421–425.  https://doi.org/10.1046/j.1365-4362.1998.00218.x CrossRefPubMedGoogle Scholar
  10. Fain A, Bochkov A (2002) On some little known and a new species of Myobiidae (Acari) associated with rodents. Bulletin de la Societe Royale Belge d’Entomologie 138:Google Scholar
  11. Feldman SH, Ntenda AM (2011) Phylogenetic analysis of Myobia musculi (Schranck, 1781) by using the 18S small ribosomal subunit sequence. Comp Med 61:484–491PubMedPubMedCentralGoogle Scholar
  12. Ferreira D, Sastre N, Ravera I, Altet L, Francino O, Bardagí M, Ferrer L (2015) Identification of a third feline Demodex species through partial sequencing of the 16S rDNA and frequency of Demodex species in 74 cats using a PCR assay. Vet Dermatol 26:239–e53.  https://doi.org/10.1111/vde.12206 CrossRefPubMedGoogle Scholar
  13. Ferrer L, Ravera I, Silbermayr K (2014) Immunology and pathogenesis of canine demodicosis. Vet Dermatol 25:427–e65.  https://doi.org/10.1111/vde.12136 CrossRefPubMedGoogle Scholar
  14. Ford CE (1966) The use of chromosome markers. In Tissue grafting and radiation. Edited by Micklem H.S., Loutit, J.F. New York: AcademicGoogle Scholar
  15. Forton FMN (2012) Papulopustular rosacea, skin immunity and Demodex: pityriasis folliculorum as a missing link. J Eur Acad Dermatol Venereol 26:19–28.  https://doi.org/10.1111/j.1468-3083.2011.04310.x CrossRefPubMedGoogle Scholar
  16. Frank LA, Kania SA, Chung K, Brahmbhatt R (2013) A molecular technique for the detection and differentiation of Demodex mites on cats. Vet Dermatol 24:367–e83.  https://doi.org/10.1111/vde.12030 CrossRefPubMedGoogle Scholar
  17. Gündüz I, López-Fuster MJ, Ventura J, Searle JB (2001) Clinal analysis of a chromosomal hybrid zone in the house mouse. Genet Res 77:41–51CrossRefPubMedGoogle Scholar
  18. Hausser J, Fedyk S, Fredga K et al (1994) Definition and nomenclature of the chromosome races of S. Araneus. Folia Zool 43:1–9Google Scholar
  19. Hill LR, Kille PS, Weiss DA, Craig TM, Coghlan LG (1999) Demodex musculi in the skin of transgenic mice. Contemp Top Lab Anim Sci 38:13–18PubMedGoogle Scholar
  20. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192.  https://doi.org/10.1093/sysbio/42.2.182 CrossRefGoogle Scholar
  21. Iijima OT, Takeda H, Komatsu Y, Matsumiya T, Takahashi H (2000) Atopic dermatitis in NC/Jic mice associated with Myobia musculi infestation. Comp Med 50:225–228PubMedGoogle Scholar
  22. Institute for Laboratory Animal Research (1991) Infectious diseases of mice and rats. In: National Academies Press. US, Washington (DC)Google Scholar
  23. Izdebska JN, Rolbiecki L (2014) Demodex lutrae n. sp. (Acari) in European otter Lutra lutra (Carnivora: Mustelidae) with data from other Demodecid mites in carnivores. J Parasitol 100:784–789.  https://doi.org/10.1645/14-532.1 CrossRefPubMedGoogle Scholar
  24. Izdebska JN, Rolbiecki L (2015) Two new species of Demodex (Acari: Demodecidae) with a Redescription of Demodex musculi and data on parasitism in Mus musculus (Rodentia: Muridae). J Med Entomol 52:604–613.  https://doi.org/10.1093/jme/tjv046 CrossRefPubMedGoogle Scholar
  25. Jacoby RO, Lindsey JR (1998) Risks of infection among laboratory rats and mice at major biomedical research institutions. ILAR J 39:266–271CrossRefPubMedGoogle Scholar
  26. Johnston NA, Trammell RA, Ball-Kell S, Verhulst S, Toth LA (2009) Assessment of immune activation in mice before and after eradication of mite infestation. J Am Assoc Lab Anim Sci 48:371–377PubMedPubMedCentralGoogle Scholar
  27. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol 11:373–384CrossRefPubMedGoogle Scholar
  28. Kawasaki T, Kawai T (2014) Toll-like receptor signaling pathways. Front Immunol 5.  https://doi.org/10.3389/fimmu.2014.00461
  29. Kethley JB (1982) Acariformes. In: Synopsis and classification of living organisms. McGraw-Hill, New York, pp 117–145Google Scholar
  30. Kethley JB, A. Norton R, M. Bonamo P, Shear W (1989) A terrestrial Alicorhagiid mite (Acari: Acariformes) from the Devonian of New York. Micropaleontology 35:367.  https://doi.org/10.2307/1485678
  31. Klompen H, Lekveishvili M, Black WC (2007) Phylogeny of parasitiform mites (Acari) based on rRNA. Mol Phylogenet Evol 43:936–951.  https://doi.org/10.1016/j.ympev.2006.10.024 CrossRefPubMedGoogle Scholar
  32. Krantz GW, Walter DE (2009) A manual of acarology: third edition, 3rd edn. Texas Tech University Press, LubbockGoogle Scholar
  33. Kumari P, Nigam R, Choudhury S, Singh SK, Yadav B, Kumar D, Garg SK (2017) Demodex canis targets TLRs to evade host immunity and induce canine demodicosis. Parasite Immunol 40.  https://doi.org/10.1111/pim.12509
  34. Lankton JS, Chapman A, Ramsay EC et al (2013) Preputial Demodex species in big brown bats (Eptesicus fuscus) in eastern Tennessee. J Zoo Wildl Med 44:124–129CrossRefPubMedGoogle Scholar
  35. Lengeling A, Pfeffer K, Balling R (2001) The battle of two genomes: genetics of bacterial host/pathogen interactions in mice. Mamm Genome 12:261–271.  https://doi.org/10.1007/s003350040001 CrossRefPubMedGoogle Scholar
  36. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lyon MF, Searle AG (1989) Genetic variants and strains of the laboratory mouse: for the international committee on standardized genetic nomenclature for mice, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  38. Mandahl N (1992) Methods in solid tumor cytogenetics. In: Human cytogenetics. A practical approach. Edited by Rooney D.E., Czepulkowski B.H., Second Edition. Oxford University Press, Oxford, New YorkGoogle Scholar
  39. Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484CrossRefPubMedGoogle Scholar
  40. Martínez-Vargas J, Muñoz-Muñoz F, Medarde N, López-Fuster MJ, Ventura J (2014) Effect of chromosomal reorganizations on morphological covariation of the mouse mandible: insights from a Robertsonian system of Mus musculus domesticus. Front Zool 11:51.  https://doi.org/10.1186/s12983-014-0051-3 CrossRefGoogle Scholar
  41. Medarde N, López-Fuster MJ, Muñoz-Muñoz F, Ventura J (2012) Spatio-temporal variation in the structure of a chromosomal polymorphism zone in the house mouse. Heredity 109:78–89.  https://doi.org/10.1038/hdy.2012.16 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Medarde N, Merico V, López-Fuster MJ, Zuccotti M, Garagna S, Ventura J (2015) Impact of the number of Robertsonian chromosomes on germ cell death in wild male house mice. Chromosome Res 23:159–169.  https://doi.org/10.1007/s10577-014-9442-8 CrossRefPubMedGoogle Scholar
  43. Mueller RS (2004) Treatment protocols for demodicosis: an evidence-based review. Vet Dermatol 15:75–89CrossRefPubMedGoogle Scholar
  44. Muñoz-Muñoz F, Sans-Fuentes MA, López-Fuster MJ, Ventura J (2011) Evolutionary modularity of the mouse mandible: dissecting the effect of chromosomal reorganizations and isolation by distance in a Robertsonian system of Mus musculus domesticus. J Evol Biol 24:1763–1776.  https://doi.org/10.1111/j.1420-9101.2011.02312.x CrossRefPubMedGoogle Scholar
  45. Murphy WJ, Eizirik E, O’Brien SJ et al (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351.  https://doi.org/10.1126/science.1067179 CrossRefPubMedGoogle Scholar
  46. Nashat MA, Luchins KR, Lepherd ML, Riedel ER, Izdebska JN, Lipman NS (2017) Characterization of Demodex musculi infestation, associated comorbidities, and topographic distribution in a mouse strain with defective adaptive immunity. Comp Med 67:315–329PubMedPubMedCentralGoogle Scholar
  47. Norris AL, Workman RE, Fan Y, Eshleman JR, Timp W (2016) Nanopore sequencing detects structural variants in cancer. Cancer Biol Ther 17:246–253.  https://doi.org/10.1080/15384047.2016.1139236 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Norton RA, Bonamo PM, Grierson JD, Shear WA (1988) Oribatid mite fossils from a terrestrial Devonian deposit near Gilboa, New York. J Paleontol 62:259–269.  https://doi.org/10.1017/S0022336000029905 CrossRefGoogle Scholar
  49. Palopoli MF, Minot S, Pei D, Satterly A, Endrizzi J (2014) Complete mitochondrial genomes of the human follicle mites Demodex brevis and D. folliculorum: novel gene arrangement, truncated tRNA genes, and ancient divergence between species. BMC Genomics 15:1124.  https://doi.org/10.1186/1471-2164-15-1124 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Parker SE, Malone S, Bunte RM, Smith AL (2009) Infectious diseases in wild mice (Mus musculus) collected on and around the University of Pennsylvania (Philadelphia) Campus. Comp Med 59:424–430PubMedPubMedCentralGoogle Scholar
  51. Piálek J, Hauffe HC, Searle JB (2005) Chromosomal variation in the house mouse. Biol J Linn Soc 84:535–563.  https://doi.org/10.1111/j.1095-8312.2005.00454.x CrossRefGoogle Scholar
  52. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  53. Pritchett-Corning KR, Cosentino J, Clifford CB (2009) Contemporary prevalence of infectious agents in laboratory mice and rats. Lab Anim 43:165–173.  https://doi.org/10.1258/la.2008.008009 CrossRefPubMedGoogle Scholar
  54. Ravera I, Altet L, Francino O, Bardagí M, Sánchez A, Ferrer L (2011) Development of a real-time PCR to detect Demodex canis DNA in different tissue samples. Parasitol Res 108:305–308.  https://doi.org/10.1007/s00436-010-2062-0 CrossRefPubMedGoogle Scholar
  55. Ravera I, Altet L, Francino O, Sánchez A, Roldán W, Villanueva S, Bardagí M, Ferrer L (2013) Small Demodex populations colonize most parts of the skin of healthy dogs. Vet Dermatol 24:168–172.e37.  https://doi.org/10.1111/j.1365-3164.2012.01099.x CrossRefPubMedGoogle Scholar
  56. Robin N, Béthoux O, Sidorchuk E, Cui Y, Li Y, Germain D, King A, Berenguer F, Ren D (2016) A carboniferous mite on an insect reveals the antiquity of an inconspicuous interaction. Curr Biol 26:1376–1382.  https://doi.org/10.1016/j.cub.2016.03.068 CrossRefPubMedGoogle Scholar
  57. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sans-Fuentes MA, López-Fuster MJ, Ventura J, Díez-Noguera A, Cambras T (2005) Effect of Robertsonian translocations on the motor activity rhythm in the house mouse. Behav Genet 35:603–613.  https://doi.org/10.1007/s10519-005-5375-5 CrossRefPubMedGoogle Scholar
  59. Sans-Fuentes MA, Muñoz-Muñoz F, Ventura J, López-Fuster MJ (2007) Rb(7.17), a rare Robertsonian fusion in wild populations of the house mouse. Genet Res 89:207–213.  https://doi.org/10.1017/S0016672307008993 CrossRefPubMedGoogle Scholar
  60. Sastre N, Ravera I, Villanueva S, Altet L, Bardagí M, Sánchez A, Francino O, Ferrer L (2012) Phylogenetic relationships in three species of canine Demodex mite based on partial sequences of mitochondrial 16S rDNA. Vet Dermatol 23:509–e101.  https://doi.org/10.1111/vde.12001 CrossRefPubMedGoogle Scholar
  61. Sastre N, Francino O, Curti JN, Armenta TC, Fraser DL, Kelly RM, Hunt E, Silbermayr K, Zewe C, Sánchez A, Ferrer L (2016) Detection, prevalence and phylogenetic relationships of Demodex spp and further skin Prostigmata mites (Acari, Arachnida) in wild and domestic mammals. PLoS One 11:e0165765.  https://doi.org/10.1371/journal.pone.0165765 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Silbermayr K, Horvath-Ungerboeck C, Eigner B, Joachim A, Ferrer L (2014) Phylogenetic relationships and new genetic tools for the detection and discrimination of the three feline Demodex mites. Parasitol Res 114:747–752.  https://doi.org/10.1007/s00436-014-4243-8 CrossRefPubMedGoogle Scholar
  63. Simon C, Frat F, Beckenbach A et al (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.  https://doi.org/10.1093/aesa/87.6.651 CrossRefGoogle Scholar
  64. Singh SK, Dimri U (2014) The immuno-pathological conversions of canine demodicosis. Vet Parasitol 203:1–5.  https://doi.org/10.1016/j.vetpar.2014.03.008 CrossRefPubMedGoogle Scholar
  65. Smith PC, Zeiss CJ, Beck AP, Scholz JA (2016) Demodex musculi infestation in genetically immunomodulated mice. Comp Med 66:278–285PubMedPubMedCentralGoogle Scholar
  66. Swofford DL (2001) Paup*: Phylogenetic analysis using parsimony (and other methods) 4.0. B5Google Scholar
  67. Tamura K, Stecher G, Peterson D, et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197
  68. Thoemmes MS, Fergus DJ, Urban J, Trautwein M, Dunn RR (2014) Ubiquity and diversity of human-associated Demodex mites. PLoS One 9:e106265CrossRefPubMedPubMedCentralGoogle Scholar
  69. Walter DE, Proctor HC (2013) Mites: ecology, evolution & behaviour: life at a microscale. Springer Science & Business MediaGoogle Scholar
  70. Woolley TA (1988) Acarology: mites and human welfare, New YorkGoogle Scholar
  71. Yamasaki K (2006) Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicdiins in skin. FASEB J 20:2068–2080.  https://doi.org/10.1096/fj.06-6075com CrossRefPubMedGoogle Scholar
  72. Zhao Y-E, Wu L-P (2012) Phylogenetic relationships in Demodex mites (Acari: Demodicidae) based on mitochondrial 16S rDNA partial sequences. Parasitol Res 111:1113–1121.  https://doi.org/10.1007/s00436-012-2941-7 CrossRefPubMedGoogle Scholar
  73. Zhao Y-E, Wu L-P, Hu L, Xu Y, Wang ZH, Liu WY (2012) Sequencing for complete rDNA sequences (18S, ITS1, 5.8S, ITS2, and 28S rDNA) of Demodex and phylogenetic analysis of Acari based on 18S and 28S rDNA. Parasitol Res 111:2109–2114.  https://doi.org/10.1007/s00436-012-3058-8 CrossRefPubMedGoogle Scholar
  74. Zhou C-F, Wu S, Martin T, Luo Z-X (2013) A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500:163–167CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Servei Veterinari de Genètica Molecular, Facultat de VeterinàriaUniversitat Autònoma de BarcelonaBarcelonaSpain
  2. 2.Human Genetics Group, Centro Nacional de Investigaciones Oncológicas (CNIO)MadridSpain
  3. 3.Departament de Biologia Animal, Biologia Vegetal i Ecologia, Facultat de BiociènciesUniversitat Autònoma de BarcelonaBarcelonaSpain
  4. 4.Departament de Ciència Animal i dels Aliments, Facultat de VeterinàriaUniversitat Autònoma de BarcelonaBarcelonaSpain
  5. 5.Vetgenomics, Parc de Recerca UAB Edifici EurekaBarcelonaSpain

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