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Variability of Fragments of Nuclear Brca1 Gene, Exon 11, and Mitochondrial Cox1 Gene in House Mice Mus Musculus A

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Variability of Fragments of Nuclear Brca1 Gene, Exon 11, and Mitochondrial Cox1 Gene in House Mice Mus Musculus A ISSN 0026-8933, Molecular Biology, 2020, Vol. 54, No. 2, pp. 185–195. © Pleiades Publishing, Inc., 2020. Russian Text © The Author(s), 2020, published in Molekulyarnaya Biologiya, 2020, Vol. 54, No. 2, pp. 212–223. GENOMICS. TRANSCRIPTOMICS UDC 599.323.45 Variability of Fragments of Nuclear Brca1 Gene, Exon 11, and Mitochondrial Cox1 Gene in House Mice Mus musculus A. S. Bogdanova, *, A. N. Maltsevb, E. V. Kotenkovab, V. G. Malikovc, A. A. Lissovskyd, V. V. Stakheeve, J. Darvishf, †, and R. Castigliag aKoltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, 119334 Russia bSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia cZoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia dZoological Museum, Moscow State University, Moscow, 125009 Russia eSouthern Scientific Center, Russian Academy of Sciences, Rostov-on-Don, 344006 Russia fFerdowsi University of Mashhad, Mashhad, 9177948974 Iran gUniversità degli Studi di Roma “La Sapienza”, Rome, 00161 Italy *e-mail: [email protected] Received June 6, 2019; revised September 27, 2019; accepted October 7, 2019 Abstract—To clarify genetic differences between subspecies of the house mouse Mus musculus, their distribu- tion, and hybridization, we first conducted a comparative analysis of variability of nucleotide sequences of fragments of the nuclear gene Brca1, exon 11 (2331 bp), and mitochondrial gene Cox1 (1260 bp) in 40 house mice from West and East Europe, Transcaucasia, Siberia, and Central and South Asia. Brca1 genotypes were divided into five main groups, which differed in a number of fixed substitutions. Genotypes of each group are characteristic for the certain geographical region and the following subspecies: M. m. musculus, M. m. domesticus, M. m. castaneus, and M. m. wagneri together with M. m. gansuensis; a fifth group corresponds to an unidenti- fied subspecies or a distinct genetic form of M. musculus from India (Sikkim State). Besides the homozygous specimens, we revealed mice, which were heterozygous for all diagnostic loci simultaneously; these speci- mens were determined as hybrid. Hybrid mice were mainly found in the zones of contact of subspecies, but in some cases, quite far from one of the parent subspecies (possibly, due to transportation). In two hybrid mice (from Bakhtiari Province of Iran and Transbaikalia of Russia), unique Brca1 haplotypes were detected. It can- not be ruled out that, at least partly, they may be characteristic of the M. m. bactrianus and M. m. gansuensis sub- species, respectively. Thus, the results of the study showed that the nuclear Brca1 gene is a promising molec- ular genetic marker for the analysis of variability, differentiation, and hybridization of house mice as well for subspecific identification of M. musculus specimens. Despite more rapid evolution of the Cox1 gene, it is not well suited for discrimination of M. m. musculus, M. m. wagneri, M. m. gansuensis specimens and Transcau- casian representatives of M. m. domesticus due to introgression and long-term maintenance of foreign mito- chondrial DNA in populations. However, Cox1 gene analysis (along with the diagnostics of animals by nuclear DNA) may be useful for estimation of population differences in M. m. castaneus and M. m. domesticus subspecies. Keywords: Mus musculus, exon 11 of Brca1 gene, Cox1, intraspecific variability and differentiation DOI: 10.1134/S0026893320020028 INTRODUCTION tics, the taxonomic system of the genus has been repeat- House mice (genus Mus) are a heterogeneous edly revised and currently is not generally accepted. Only group that includes numerous forms in varying the species level of the differences between the “wild” degrees differing from one another in morphological, house mice in relation to the synanthropic house mice ecological, ethological features and genetic character- can be recognized as indisputable. The “wild” forms (the istics. Due to the high diversity, asynchronous vari- Macedonian mouse M. macedonicus, the steppe mouse ability of morphological and genetic traits, and due to M. spicilegus, and the Western Mediterranean mouse hybridization of synanthropic forms, which consider- M. spretus) are also currently identified by the majority ably complicates distinguishing discrete population of researchers [1–3] as allospecies; i.e., their status in groups and determination of their specific characteris- fact is equal to the species. Numerous parapatric synanthropic forms are com- † Deceased. bined in the house mouse species, M. musculus (or 185 186 BOGDANOV et al. superspecies, from a different point of view). Their evolve much faster than nuclear genes [19–21]. taxonomy remains controversial despite the fact that Apparently, for this reason, the nuclear genes were M. musculus is one of the main laboratory objects of studied (except for several mentioned papers) when genetic and molecular biological research, and its com- comparing species of house mice and the most distinct plete genome was sequenced second after the human M. musculus subspecies in a limited number of animals genome [4]. Typically, the synanthropic forms of the [13, 22–24]. However, the analysis of mtDNA, which house mouse are considered as subspecies [2, 3, 5–8], has a different mode of inheritance (is transmitted to although it has been proposed to rise the taxonomic rank descendants through the egg cytoplasm, i.e., by the of some of them (M. m. domesticus, M. m. castaneus, and maternal line) and recombines neither with other M. m. musculus) to species [9–13]. Until recently, con- mtDNA molecules nor with nDNA, can reveal a tradictory information was also published about the mixed composition of the population but does not Central Asian subspecies M. m. wagneri and Transbai- make it possible to identify a hybrid origin of individ- kalian M. m. gansuensis, which were considered mor- uals without using nuclear markers. Thus, the discrep- phologically and genetically closest to M. m. musculus. ancy between the results of identification by karyo- For example, according to Spiridonova et al. [14], all typic, nuclear markers, on the one hand, and mito- M. musculus subspecies can be identified by the com- chondrial markers, on the other hand, is not surprising plex of RAPD-PCR markers, and the level of differ- and may even be expected, especially in hybrid zones. ences between some of them (M. m. wagneri and In this regard, it seems necessary to analyze the most M. m. musculus) is comparable to interspecies differ- rapidly evolving nuclear autosomal genes. Therefore, ences. In addition, successful identification of individuals the selection of a suitable nuclear marker exhibiting of M. m. wagneri, M. m. gansuensis, and M. m. musculus specificity in all or at least in the majority of intraspe- by karyotypic characters was reported [15]. However, cific forms of M. musculus (which is required for the analysis of variability of the second intron of the studying hybridization) and population variability to nuclear hemoglobin b1 chain gene (Hbb-b1) revealed analyze genetic polymorphism is of paramount only two genotypes in the house mice of Central Asia importance. and Transbaikalia, one of which was identified as The main purpose of this study was to investigate characteristic of M. m. musculus, and the other was the genetic diversity of house mice from several popu- found to be common for M. m. wagneri and M. m. gan- lations of Europe, Transcaucasia, Central Asia, and suensis [16]. Likewise, in the study of polymorphism of Siberia by the nucleotide sequence of a fragment of eight linked genes of the eighth autosome, two phy- exon 11 of the autosomal nuclear gene Brca1 (Breast logroups of house mice (“musculus” and “wagneri”) Cancer 1) as well as to assess the suitability of this were identified in Asia [17]. The results of recent stud- marker for the analysis of phylogenetic relationships ies of mtDNA fragments—the control region (D-loop) and hybridization of intraspecific forms of M. muscu- and the cytochrome b gene (Cytb)—showed a com- lus. In addition to the Brca1 gene, in some individuals plete, approximately the same, though noticeably infe- we sequenced a fragment of the mitochondrial gene rior to the allospecies of “wild” mice, genetic differen- encoding the first subunit of cytochrome oxidase tiation of the subspecies M. m. domesticus, M. m. mus- (Cox1) to determine the level of polymorphism of this culus, M. m. castaneus, M. m. gentilulus, M. m. bactrianus, marker in the group of house mice, to refine the a new subspecies M. m. isatissus, and an unclassified genetic differences identified as a result of analysis of form from Nepal [7, 8, 16, 17]. However, despite the the Brca1 gene, and to additionally verify the hybrid rather high variability of the mitochondrial genes, origin of some specimens. the subspecies M. m. musculus, M. m. wagneri, and M. m. gansuensis did not form individual clades on dendrograms [7, 16–18]. Distinguishing subclusters, MATERIALS AND METHODS which often included mice originating from very dis- In total, we studied 40 individuals tant regions and belonging to different subspecies, had M. musculus belonging to at least five subspecies: , an apparently random nature. It was assumed that the M. m. musculus , , , and mtDNA in the subspecies and M. m. wagneri M. m. gansuensis M. m. domesticus M. m. wagneri . Two Macedonian mice ( was substituted with the mtDNA of M. m. castaneus M. macedoni- M. m. gansuensis ) and one steppe mouse ( ) were used as as a result of “absorbing” hybridiza- cus M. spicilegus M. m. musculus outgroups. The localities where mice were caught, the tion [16]. Due to the limited genetic evidence in favor composition of samples in which and of isolation of and with Brca1 Cox1 M. m. wagneri M. m. gansuensis genes were studied, and the accession numbers of the respect to both each other and , in the M. m. musculus nucleotide sequences deposited in the GenBank data- checklist on mammals of the world fauna [3] the first base are shown in Table 1.
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