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 ¼ 22, Standard, St: 2n ¼ 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 ¼ 40, 2n ¼ 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.

Chromosomal polymorphism in mammals: an evolutionary perspective

“…Modifying chromosome arm length and/or number, as well as centromere location, are clearly expected to have an impact on recombination patterns since at least one chiasma per chromosomal arm has to form during mammalian meiosis for the proper segregation of homologs (de Villena & Sapienza, 2001b). Accordingly, empirical studies have shown that Rb metacentrics modify the number and distribution of chiasmata in the genomes of house mice (Bidau et al, 2001;Castiglia & Capanna, 2002;Dumas & Britton-Davidian, 2002;Merico et al, 2013;Dumas, Catalan & Britton-Davidian, 2014), as well as marsh rats (Nachman, 1992), tuco-tucos (Basheva et al, 2014) and shrews (Borodin et al, 2008).…”

“…Stefansson et al, 2005;Ma & Amos, 2012), most empirical evidence in mammals has dealt with the effects of Rb fusions on recombination patterns (e.g. Merico et al, 2013;Basheva et al, 2014;Dumas et al, 2014). Another interesting situation exists in the common shrew where the metacentric pair tu (i.e.…”

Effect of species-specific differences in chromosome morphology on chromatin compaction and the frequency and distribution of RAD51 and MLH1 foci in two bovid species: cattle (Bos taurus) and the common eland (Taurotragus oryx)

“…The number of MLH1 foci on the BTA2 orthologue located distally on the same chromosome arm in the common eland did not significantly differ from the BTA2 in cattle. Such a suppression of class I COs in rearranged chromosome regions can cause a reduction in genetic variability; however, it can prevent the disruption of favourable allelic combinations in genes that are newly linked in karyotype evolution and enable the accumulation of genetic incompatibilities in the process of speciation (Butlin 2005;Dumas et al 2015).…”

Chromosomes and speciation in tuco-tuco (Ctenomys, Hystricognathi, Rodentia)

“…В то же время получены свидетельства в пользу современной версии этой гипотезы. Существенные изменения в реком-бинации наблюдались у мышей и землероек -носителей простых и сложных гетерозигот по робертсоновским транслокациям по сравнению с гомозиготами (Searle, 1986(Searle, , 1993Wallace et al, 1992;Bidau et al, 2001;Dumas, BrittonDavidian, 2002;Borodin et al, 2008;Merico et al, 2013;Dumas et al, 2015).…”