Skin mites in mice (Mus musculus): high prevalence of Myobia sp. (Acari, Arachnida) in Robertsonian mice
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.
KeywordsSkin mites Myobia Demodex Robertsonian fusions Mouse Prevalence
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.
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).
- 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
- 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
- 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
- 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
- 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
- Institute for Laboratory Animal Research (1991) Infectious diseases of mice and rats. In: National Academies Press. US, Washington (DC)Google Scholar
- Kawasaki T, Kawai T (2014) Toll-like receptor signaling pathways. Front Immunol 5. https://doi.org/10.3389/fimmu.2014.00461
- Kethley JB (1982) Acariformes. In: Synopsis and classification of living organisms. McGraw-Hill, New York, pp 117–145Google Scholar
- 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
- Krantz GW, Walter DE (2009) A manual of acarology: third edition, 3rd edn. Texas Tech University Press, LubbockGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Swofford DL (2001) Paup*: Phylogenetic analysis using parsimony (and other methods) 4.0. B5Google Scholar
- 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
- Walter DE, Proctor HC (2013) Mites: ecology, evolution & behaviour: life at a microscale. Springer Science & Business MediaGoogle Scholar
- Woolley TA (1988) Acarology: mites and human welfare, New YorkGoogle Scholar
- 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