Linkage-dependent gene flow in a house mouse chromosomal hybrid zone

In the alpine valley of Valtellina there are two Robertsonian chromosomal races of house mouse, the Poschiavo (POS: 2n = 24-26) characterized by metacentric 8.12 and acrocentrics 2 and 10 and the Upper Valtellina (UV: 2n = 22-24) characterized by metacentrics 2.8 and 10.12. The races inhabit separate villages in the valley except in Sommacologna and Sondalo, where they both occur together with hybrids. A total of 179 mice from 16 villages were typed at 13 microsatellite loci. Seven of these loci were localized close to the centromeres of chromosomes 10 and 12, with the prediction that these regions on the race-specific chromosomes would be the most likely to experience a barrier to gene flow. The remaining six loci were localized at the telomeres of chromosomes 10 and 12 and at the centromeres of chromosomes that do not differ between the races. Substantial differences in allelic frequencies were found between the villages with POS and UV races at five of the loci at the centromeres of chromosomes 10 and 12 but at none of the other loci. These differences were not found to distinguish the two races in Sommacologna and Sondalo. Therefore, the centromeric regions of race-specific chromosomes do appear to experience a barrier to gene flow, although this can break down under intense interbreeding between the races. These results are considered in the context of Harrison's (1990) concept of the semipermeability of hybrid zones to gene exchange and in relation to parapatric speciation.     

The tobacco mouse and its relatives: a "tail" of coat colors, chromosomes, hybridization and speciation

The article reviews over 30 years' study of the chromosomal variation of the western house mice (Mus musculus domesticus) from the neighboring valleys of Poschiavo and Valtellina on the Swiss-Italian border. This is done in the context of the social and political history of this area, on the grounds that mice, as commensals, are influenced by human history. The chromosomal study of mice in this area was initiated because their unusual black coat color led a 19th century naturalist to describe the "tobacco mice" from Val Poschiavo as a separate species (Mus poschiavinus). The special coloration of the Val Poschiavo mice is matched by their chromosomes: they have 26 chromosomes instead of the usual 40. The Val Poschiavo mice are not a separate species according to the Biological Species Concept; instead they constitute a chromosome race (the "Poschiavo", POS) that is related to other races with reduced chromosome numbers that occur in N Italy (of which only those races in Val Poschiavo and Upper Valtellina have black coats). A phylogenetic analysis of mitochondrial DNA sequences suggests that the lineage of chromosome races found in N Italy was not formed during an extreme population bottleneck, although such bottlenecks have apparently occurred during the origin of individual races and certainly have influenced single populations. In one small, isolated population in Valtellina (Migiondo), two chromosome races (the POS and the "Upper Valtellina", UV, 2n = 24) became reproductively isolated from each other. In another small population (Sernio) bottlenecking led to fixation of a hybrid form with the UV karyotype and coat color, but with allozyme and microsatellite alleles characteristic of mice with the standard 40-chromosome karyotype. Two of the chromosome races in Valtellina (the UV and the "Mid Valtellina", MV, 2n = 24) also appear to be the product of hybridization. The dynamic history and patchy distribution of the house mouse chromosome races in Val Poschiavo and Valtellina in part reflects extinction-recolonization events; the formation of the UV and MV races and the introduction of the pale brown Standard race mice are believed to reflect such events. Dynamism in the chromosomal constitution of single populations is also evident from 25 years of data on the population in Migiondo. Due to change in agricultural practices, house mice in Valtellina and Val Poschiavo are becoming rarer, which is likely to have further impacts on the distribution and characteristics of the chromosome races in this area.     

Empirical demonstration of hybrid chromosomal races in house mice

Western house mice (Mus musculus domesticus) and common shrews (Sorex araneus) are important models for study of chromosomal speciation. Both had ancestral karyotypes consisting of telocentric chromosomes, and each is subdivided into numerous chromosomal races many of which have resulted from fixation of new mutations (Robertsonian fusions and whole‐arm reciprocal translocations). However, some chromosomal races in both species may alternatively have originated through hybridization, with particular homozygous recombinant products reaching fixation. Here, we demonstrate the process of generation of hybrid chromosomal races for the first time in either species using molecular markers. Analysis of centromeric microsatellite markers show that the Mid Valtellina (IMVA) and Upper Valtellina (IUVA) chromosomal races of the house mouse are recombinant products of hybridization of the Lower Valtellina (ILVA) and Poschiavo (CHPO) chromosomal races, supporting earlier theoretical analysis. IMVA and IUVA occupy a small area of the Italian Alps where ILVA makes contact with CHPO. IUVA and CHPO have previously been shown to be reproductively isolated in one village, emphasizing that hybrid chromosomal races in small mammals, as in plants, have the potential to be part of the speciation process.     

UNDERSTANDING THE BASIS OF DIMINISHED GENE FLOW BETWEEN HYBRIDIZING CHROMOSOME RACES OF THE HOUSE MOUSE

Speciation may be promoted in hybrid zones if there is an interruption to gene flow between the hybridizing forms. For hybridizing chromosome races of the house mouse in Valtellina (Italy), distinguished by whole‐arm chromosomal rearrangements, previous studies have shown that there is greater interruption to gene flow at the centromeres of chromosomes that differ between the races than at distal regions of the same chromosome or at the centromeres of other chromosomes. Here, by increasing the number of markers along race‐specific chromosomes, we reveal a decay in between‐race genetic differentiation from the centromere to the distal telomere. For the first time, we use simulation models to investigate the possible role of recombination suppression and hybrid breakdown in generating this pattern. We also consider epistasis and selective sweeps as explanations for isolated chromosomal regions away from the centromere showing differentiation between the races. Hybrid breakdown alone is the simplest explanation for the decay in genetic differentiation with distance from the centromere. Robertsonian fusions/whole‐arm reciprocal translocations are common chromosomal rearrangements characterizing both closely related species and races within species, and this fine‐scale empirical analysis suggests that the unfitness associated with these rearrangements in the heterozygous state may contribute to the speciation process.