CENTROMERIC INCOMPATIBILITIES IN THE HYBRID ZONE BETWEEN HOUSE MOUSE SUBSPECIES FROM DENMARK: EVIDENCE FROM PATTERNS OF NOR ACTIVITY.

Abstract

The introgression pattern of centromeric nucleolar organizer regions (NORs) was studied in house mice from the hybrid zone between Mus musculus musculus and Mus musculus domesticus in Denmark. In this region, the two subspecies are chromosomally differentiated: M. m domesticus carries three pairs of Robertsonian (Rb) fusion chromosomes (2n = 34), while M. m. musculus exhibits the ancestral karyotype of 2n = 40 acrocentric chromosomes. A previous chromosomal analysis showed that the Rb clines were staggered and nonconcordant, and that the Rb fusions did not introgress into the M. m. musculus genome due to incompatibilities involving only the centromeric regions. In the present study, the distribution of a centromeric NOR cluster located on an acrocentric chromosome not involved in the Rb fusions (chromosome 11; NOR11 ) was investigated to determine if the observed centromeric incompatibilities were limited to the chromosomal rearrangements or were related to centromeric differentiation between the subspecies. The cytogenetic study by silver staining documented the activity pattern of the five major NOR-bearing chromosome pairs (12, 15, 16, 18, and 19) common to both subspecies and confirmed presence of NOR11 in M. m. musculus and absence in M. m. domesticus. The NOR11 activity pattern showed a very narrow and off-centered clinal transition. An in situ hybridization analysis with rDNA probes indicated that the decrease in frequency of activity of NOR11 through the hybrid zone was related to absence of ribosomal genes in this cluster and not to transcription repression due to competitive or dominance interactions. The center of the NOR11 cline was significantly different from that of the consensus allozymic markers, but coincided with that of the steepest Rb cline. Several arguments support the view that the selective processes involved in maintaining the NOR11 cline are related to the centromeric region of these chromosomes. These include: (1) the similarity in shape and position of the Rb and NOR11 clines; (2) the absence of activity dysfunction involving NOR11 ; and (3) the tight linkage between NORs and centromeres in house mice. This study indicates that the centromeric segments of acrocentric chromosomes not involved in chromosomal rearrangements show incompatibilities similar to those evidenced by the Rb fusions. These centromeric incompatibilities are thus more likely related to centromeric origin and subspecific differentiation (domesticus vs. musculus) than to centromeric rearrangement (Rb vs. non-Rb). In this case, it may be predicted that the selective processes maintaining the chromosomal clines are distributed over many, if not all, the centromeres and may combine . to limit the gene flow between M. m. domesticus and M. m. musculus.