Origin of the chromosomal radiation of Madeiran house mice: a microsatellite analysis of metacentric chromosomes

Abstract

Chromosome races of Mus musculus domesticus are characterised by particular sets of metacentric chromosomes formed by Robertsonian fusions and whole-arm reciprocal translocations. The Atlantic island of Madeira is inhabited by six chromosome races of house mice with 6-9 pairs of metacentric chromosomes. Three of these races are characterised by the metacentric 3.8 also found elsewhere in the distribution of M. m. domesticus, including Denmark and Spain. We investigated the possibility that metacentric 3.8 was introduced to Madeira during the initial colonisation, as this could have 'seeded' the cascade of chromosomal mutation that is the basis of the extraordinary chromosomal radiation observed on the island. Variation at 24 microsatellite loci mapping to three different chromosomal regions (proximal, interstitial and distal) of mouse chromosomes 3 and 8 was investigated in 179 mice from Madeira, Denmark, Portugal, Spain, Italy and Scotland. Analyses of microsatellite loci closely linked to the centromeres of these chromosomes ('proximal loci') do not support a common evolutionary origin of metacentric 3.8 among Madeiran, Danish and Spanish mouse populations. Our results suggest that Madeiran mice are genetically more similar to standard karyotype mice from Portugal than to metacentric mice from elsewhere. There is expected to be an interruption to gene flow between hybridising metacentric races on Madeira, particularly in the chromosomal regions close to the rearrangement breakpoints. Consistent with this, relating to differentiation involving chromosomes 3 and 8 on Madeira, we found greater genetic structure among races for proximal than interstitial or distal loci.

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

“…However, several studies have addressed this question by measuring the level of divergence of mapped microsatellite markers between chromosomally differentiated house mice. In all cases, centromeric loci exhibited higher differentiation levels than distal ones, regardless of the type of meiotic heterozygosity of the hybrids, that is, complex chains or rings (Panithanarak et al, 2004;Förster et al, 2013;Gimenez et al, 2013 ) or trivalents (Franchini et al, 2010). Previous studies have indicated that recombination suppression extended up to 15-20 cM from the centromere depending on the chromosomes involved in the Rb fusion and the genetic background (Davisson and Akeson, 1993;Gimenez et al, 2013;Capilla et al, 2014).…”

Differing Y chromosome versus mitochondrial DNA ancestry, phylogeography, and introgression in the house mouse

“…Nuclear sequence data, including from the Y chromosome, have often been used for studies involving multiple subspecies or species (Boissinot & Boursot, ; Geraldes et al ., ) but not generally extended to within‐subspecies phylogeographical history, often as a result of insufficient polymorphism. Where more recent phylogeographical studies have used additional non‐mtDNA markers, these have tended to be autosomal microsatellites that have been useful to examine population‐level genetic parameters of the study populations but, so far, they are of less value for inferring colonization history (Hardouin et al ., ; Jones et al ., , b, ; Förster et al ., ; Gabriel, Mathias & Searle, ). There is further potential for nuclear studies from large‐scale house mouse single nucleotide polymorphism arrays (Yang et al ., ); these could provide a reliable phylogeographical history for the autosomes, although the cost of the chips may be prohibitive for phylogeographical studies.…”

Mammalian Meiotic Recombination: A Toolbox for Genome Evolution

“…Boro-din et al [2008] detected a reduction in CO frequency in translocated chromosomes of the common shrew, whereas others reported a reduction in both chiasmata number and COs in house mice due to Robertsonian translocations [Castiglia and Capanna, 2002;Dumas and BrittonDavidian, 2002;Capilla et al, 2014]. On the contrary, indirect evidence for the suppression of recombination has included the analysis of rates of genetic divergence and recombination between rearranged and collinear chromosomes [Navarro and Barton, 2003;Franchini et al, 2010;Farré et al, 2013;Förster et al, 2013;Giménez et al, 2013]. This latter approach has been used in several studies on Drosophila [Kulathinal et al, 2008], Helianthu s sp.…”