Adaptive introgressive hybridization with the Algerian mouse (Mus spretus) promoted the evolution of anticoagulant rodenticide resistance in European house mice (M. musculus domesticus)

Abstract

Adaptive introgressive hybridization refers to the natural transfer of genes after interspecific mating between species, and subsequent expression of these genes in the recipient species as a new trait that confers selective advantages. Conceptually, the process harnesses immense potential to explain rapid evolution of traits. However, the process requires that reproductive isolation be overcome. Here we present a case of the adaptive introgression of anticoagulant rodenticide resistance from the Algerian mouse (Mus spretus Lataste, 1883) to the Western European house mouse (M. musculus domesticus Linnaeus, 1758). These once allopatric species have come into secondary geographic contact and hybridize occasionally. However, only for an approximately ~20.3 megabase-sized genomic fragment, carrying the vitamin K 2,3-epoxide reductase subunit 1 gene (vkorc1) of M. spretus (vkorc1spr), has hybridization resulted in introgression into the M. m. domesticus genome. This vkorc1spr allele carries amino-acid substitutions, conferring resistance to anticoagulants, has evolved under positive selection in M. spretus (Ka/Ks=1.54-1.93) and displays adaptive population genetic dynamics in M. m. domesticus populations. Since its natural inception <60 years ago, this novel form of pesticide-resistant mice has spread far into the range of M. m. domesticus. Other vkorc1 resistance alleles now known to occur in European house mice originated either by de novo mutation or from standing genetic variants. Recombinants between these and introgressed alleles are now emerging, but the role of such novel alleles in resistance has yet to be established. Our snapshot of the ongoing adaptive introgression of vkorc1spr illustrates how hybridization, coinciding with strong selection with anticoagulants, resulted the breakdown of reproductive barriers between M. spretus and house mice. Pest control should anticipate the possibility of horizontal gene transfer between closely related rodent species as a mechanisms leading to rodenticide resistance.

Keywords

• genetic introgression
• hybridization
• vitamin K epoxide reductase subcomponent 1
• vkorc1