Surrounded by Kindred: Spermophilus major Hybridization with Other Spermophilus Species in Space and Time

Biology (Basel). 2023 Jun 17;12(6):880. doi: 10.3390/biology12060880.

Abstract

Among the numerous described cases of hybridization in mammals, the most intriguing are (a) cases of introgressive hybridization deeply affecting the evolutionary history of species, and (b) models involving not a pair of species but a multi-species complex. Therefore, the hybridization history of the russet ground squirrel Spermophilus major, whose range has repeatedly changed due to climatic fluctuations and now borders the ranges of four related species, is of great interest. The main aims of this study were to determine the direction and intensity of gene introgression, the spatial depth of the infiltration of extraneous genes into the S. major range, and to refine the hypothesis of the hybridogenic replacement of mitochondrial genomes in the studied group. Using phylogenetic analysis of the variability of mitochondrial (CR, cytb) and nuclear (SmcY, BGN, PRKCI, c-myc, i6p53) markers, we determined the contribution of neighboring species to the S. major genome. We showed that 36% of S. major individuals had extraneous alleles. All peripheral species that were in contact with S. major contributed towards its genetic variability. We also proposed a hypothesis for the sequence and localization of serial hybridization events. Our assessment of the S. major genome implications of introgression highlights the importance of implementing conservation measures to protect this species.

Keywords: Spermophilus; hybridization; introgression; mitochondrial genome; nuclear genome; russet ground squirrel; secondary contact zone; speciation.