Fertility assessment in hybrids between monobrachially homologous Rb races of the house mouse from the island of Madeira: implications for modes of chromosomal evolution

Abstract

The speciation model of divergence by monobrachially homologous fusions (that is, with one arm in common) benefits from a wide conceptual acceptance, because heterozygotes between populations carrying such fusions suffer from high levels of meiotic dysfunction. The same meiotic configurations can also be generated by WART (whole-arm reciprocal translocation), rearrangements that are known to occur in mammals. Estimating the disadvantage of heterozygotes carrying monobrachially homologous fusions is required to evaluate the relevance of this mode of chromosomal evolution in diversification and speciation. House mice are an excellent study models because chromosomal races exist carrying monobrachially homologous fusions, and WARTs have been documented in this species. The fertility of heterozygote mice carrying the smallest number of monobrachially homologous fusions (that is, a chain of four chromosomes, C4) was investigated in laboratory-bred hybrids between two parapatric chromosomal races from the island of Madeira. Meiotic nondisjunction analyses and histological sections of testes showed that aneuploidy (16.7%) and germ cell death (50.9%) rates reached significantly higher mean values in hybrids than in homozygotes. In females, however, the histological analysis of ovarian follicle parameters revealed no significant differences between hybrid and homozygous individuals. Overall, the reproductive assays indicated that these C4-carrying hybrids were not sterile but showed an approximately 50% decrease in fertility compared to homozygous parental mice. Implications for modes of chromosomal evolution involving monobrachially homologous fusions are discussed.

The frequency of heterologous synapsis increases with aging in Robertsonian heterozygous male mice

“…This extraordinary variability is produced either by Robertsonian translocation ((Rb) two telocentric chromosomes fuse at the centromeric regions producing a metacentric chromosome), or by whole arm reciprocal translocation (between Rb chromosomes or an Rb and a telocentric chromosome) (Capanna and Redi 1995;Pialek and Albrecht 2005). The presence of Rb chromosomes in heterozygosity has detrimental effects on spermatogenesis, giving rise to subfertility or complete sterility (Redi and Capanna 1988;Garagna et al 1990Garagna et al , 2001bWallace et al 1992Wallace et al , 2002Everett et al 1996;Hauffe and Searle 1998;Merico et al 2003;Manterola et al 2009;Nunes et al 2011). During meiosis, Rb heterozygosities produce intricated prophase I figures, like long chains, rings or trivalents, which show mainly asynapsis, among several other synaptic defects (Johannisson and Winking 1994;Wallace et al 2002;Manterola et al 2009).…”

Genetic recombination variation in wild Robertsonian mice: on the role of chromosomal fusions andPrdm9allelic background

“…Under this 'suppressed recombination' model, chromosome reorganizations in heterokaryotypes have a minimal influence on fitness, but rather affect recombination thus contributing to a reduction of gene flow within these genomic regions and the consequent accumulation of genetic incompatibilities [3]. Data supporting recombination suppression by inversions have been reported in different model organisms (see [4] and references therein), whereas studies regarding the effects of fusions have been restricted to the western house mouse, Mus musculus domesticus [5][6][7][8][9][10][11][12][13][14] and the common shrew, Sorex araneus [15,16]. The general view is that chromosomal reorganizations disturb the chromosomal distribution of recombinational events altering, in the long term, the final outcome of crossovers (COs).…”

Spatio-temporal variation in the structure of a chromosomal polymorphism zone in the house mouse

“…By contrast, the accumulation of numerous Rb translocations is related to hybrid hypofertility or sterility as a result of alterations in meiotic processes (Wallace et al, 1992;Castiglia and Capanna, 2000). Therefore, high heterozygosity for rearrangements is expected to reduce the fitness of hybrid mice, thus limiting the gene flow between races (Hauffe and Searle, 1998;Nunes et al, 2011).…”