Reduced recombination patterns in Robertsonian hybrids between chromosomal races of the house mouse: chiasma analyses

Abstract

The recombination suppression models of chromosomal speciation posit that chromosomal rearrangements act as partial barriers to gene flow allowing these regions to accumulate genetic incompatibilities, thus contributing to the divergence of populations. Empirical and theoretical studies exploring the requirements of these models have mostly focused on the role of inversions. Here, the recombination landscape of heterozygosity for Robertsonian (Rb) fusions is investigated in the house mouse. Laboratory-bred F1 males and females between highly differentiated races from Tunisia (Rb: 2n=22, Standard, St: 2n=40) were produced in which all Rb fusions are present as trivalents in meiosis. Recombination patterns were determined by the analysis of chiasmata and compared with previous data on the Tunisian parental mice. A comparative analysis was performed on wild-caught male mice spanning the hybrid zone between two Italian races (2n=40, 2n=22). The results showed that the chiasma characteristics of both male and female Tunisian F1 and Italian hybrids clearly differed from those of Rb and St mice. Not only was the mean chiasma number (CN) intermediate between those of the parental mice in both geographic samples, but the distribution of chiasmata along the chromosomal arms of the F1 showed a distinct mosaic pattern. In short, the proximal region in the F1 exhibited a reduced CN similar to that observed in homozygous Rb, whereas distal regions more closely matched those in St mice. These results suggest that Rb rearrangements (homozygous or heterozygous) reduce recombination in the proximal regions of the chromosomes supporting their potential role in recombination-mediated speciation models.

Figure 1

Metaphase I plates of F1 Tunisian mice. (a) female F1; (b) male F1.

Figure 2

Distribution of mean autosomal chiasma number per cell (CN) according to diploid number in the Italian wild-caught and F1 male mice. Rb=22, St=40, 31=laboratory-bred F1. Data for the Rb and St Tunisian mice are from Dumas and Britton-Davidian (2002).

Figure 3

Mean per cell distribution of chiasmata along 10% segments of the autosomal arms in Tunisian (a) males and (b) females (data for the Rb and St Tunisian mice are are from Dumas and Britton-Davidian, 2002), and (c) Rb and St Italian wild-caught males. The three regional distributions are indicated: proximal (0–50%), distal (50–90%), terminal (90–100%). Cent: centromere; Telo: telomere.

Figure 4

Cumulative probability of the occurrence of allelic exchanges during meiosis between homologous chromosomes relative to the location on the chromosomal arm (10% segments), the karyotype and the sex of the animal. The data are estimated from CN values and distribution of the Tunisian mice (F1: present study; Rb and St: Dumas and Britton-Davidian, 2002). Rb=Rb homozygotes; St=standard populations. The three regional distributions are indicated: proximal (0–50%), distal (50–90%), terminal (90–100%). Centro: centromere; Telo: telomere.