Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Abstract Background Western house mice Mus musculus domesticus are among the most important mammalian model species for chromosomal speciation. Hybrids between chromosomal races of M. m. domesticus suffer various degrees of fertility reduction between full fertility and complete sterility, depending on the complexity of the chromosomal differences between the races. This complexity presents itself in hybrids as meiotic configurations of chromosome chains and rings, with longer configurations having a stronger impact on fertility. While hybrids with short configurations have been intensively studied, less work has been done on hybrids with very long configurations. In this study, we investigated laboratory-reared wild mice from two chromosomally very different races in Switzerland found in close proximity. Hybrids between these races form a meiotic chain of fifteen chromosomes. We performed a detailed analysis of male and female hybrid fertility, including three generations of female backcrosses to one of the parental races. We also tested for possible divergence of mate preference in females. Results While all male F1 hybrids were sterile with sperm counts of zero, 48% of female F1 hybrids produced offspring. Their litter sizes ranged from one to three which is significantly lower than the litter size of parental race females. When hybrid females were backcrossed to a parental race, half of the offspring resembled the parental race in karyotype and fertility, while the other half resembled the F1 hybrids. In the preference test, females of both races indicated a lack of a preference for males of their own karyotype. Conclusions Although the fertility of the F1 hybrids was extremely low because of the complexity of the chromosomal differences between the races, reproductive isolation was not complete. As we did not find assortative female preferences, we expect that contact between these races would lead to the production of hybrids and that gene flow would occur eventually, as fertility can be restored fully after one backcross generation

Chromosomal Variation and Its Effects on Reproductive Isolation in the Western House Mouse Mus musculus domesticus

The origin of species is one of the central questions in evolutionary biology. Mayr (1995) defined species as groups of interbreeding natural populations which are reproductively isolated from one another. One of the potential reproductive barriers is the chromosomal rearrangement. Species, even closely related ones or even races within species, may differ drastically in number and composition of their chromosomes. When different chromosomal variants hybridize, their hybrids may suffer a reduced fertility due to problems arising during meiosis. In addition, chromosomal rearrangements can change the linkage between genes that may can lead to reproductive isolation. In this thesis, I study the effect of Robertsonian translocations, a common chromosomal rearrangement in which two acrocentric chromosomes fuse into a metacentric, on reproductive isolation in wild western house mice Mus musculus domesticus. Hybrids between chromosomal races of house mice suffer various degrees of fertility reduction, from no reduction to complete sterility, depending on the complexity of the chromosomal differences between their parental races. The majority of research has focused on hybrids with lower complexity, however here I investigate hybrids with higher chromosomal complexity. My results show that even a very high complexity of chromosomal variation between chromosomal house mouse races does not lead to complete reproductive isolation, as female hybrids retained some fertility, albeit greatly reduced (Chapter I). The investigation of a possible effect of Rb translocations on recombination showed that they had the potential to reduce gene flow, even though no significant effect on recombination frequency was found. (Chapter II). Genetic analysis of wild chromosomal races confirmed that differences in Rb translocations between chromosomal races influenced genetic differentiation, with increased linkage and differentiation near centromeres of Rb translocation not shared between races (Chapter III). All results together show that fertility decrease and the accumulation of different Rb translocations have the potential to change genetic linkage and provide regions of increased genetic differentiation, and thus may ultimately play a role in the reproductive isolation of chromosomal races

Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Background Western house mice Mus musculus domesticus are among the most important mammalian model species for chromosomal speciation. Hybrids between chromosomal races of M. m. domesticus suffer various degrees of fertility reduction between full fertility and complete sterility, depending on the complexity of the chromosomal differences between the races. This complexity presents itself in hybrids as meiotic configurations of chromosome chains and rings, with longer configurations having a stronger impact on fertility. While hybrids with short configurations have been intensively studied, less work has been done on hybrids with very long configurations. In this study, we investigated laboratory-reared wild mice from two chromosomally very different races in Switzerland found in close proximity. Hybrids between these races form a meiotic chain of fifteen chromosomes. We performed a detailed analysis of male and female hybrid fertility, including three generations of female backcrosses to one of the parental races. We also tested for possible divergence of mate preference in females. Results While all male F1 hybrids were sterile with sperm counts of zero, 48% of female F1 hybrids produced offspring. Their litter sizes ranged from one to three which is significantly lower than the litter size of parental race females. When hybrid females were backcrossed to a parental race, half of the offspring resembled the parental race in karyotype and fertility, while the other half resembled the F1 hybrids. In the preference test, females of both races indicated a lack of a preference for males of their own karyotype. Conclusions Although the fertility of the F1 hybrids was extremely low because of the complexity of the chromosomal differences between the races, reproductive isolation was not complete. As we did not find assortative female preferences, we expect that contact between these races would lead to the production of hybrids and that gene flow would occur eventually, as fertility can be restored fully after one backcross generation

Additional file 7: of Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Data of female preference test. (XLSX 17 kb

Additional file 4: of Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Data of female fertility. (XLSX 13 kb

Additional file 5: of Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Data of litter sizes for all litters of hybrid and control females. (XLSX 14 kb

Additional file 3: of Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Data of male fertility. (XLSX 20 kb

Additional file 6: of Measurements of hybrid fertility and a test of mate preference for two house mouse races with massive chromosomal divergence

Data of sperm counts of males used in female backcrosses. (XLSX 10 kb

R2d2 drives selfish sweeps in the house mouse

A selective sweep is the result of strong positive selection driving newly occurring or standing genetic variants to fixation, and can dramatically alter the pattern and distribution of allelic diversity in a population. Population-level sequencing data have enabled discoveries of selective sweeps associated with genes involved in recent adaptations in many species. In contrast, much debate but little evidence addresses whether "selfish" genes are capable of fixation - thereby leaving signatures identical to classical selective sweeps - despite being neutral or deleterious to organismal fitness. We previously described R2d2, a large copy-number variant that causes nonrandom segregation of mouse Chromosome 2 in females due to meiotic drive. Here we show population-genetic data consistent with a selfish sweep driven by alleles of R2d2 with high copy number (R2d2) in natural populations. We replicate this finding in multiple closed breeding populations from six outbred backgrounds segregating for R2d2 alleles. We find that R2d2 rapidly increases in frequency, and in most cases becomes fixed in significantly fewer generations than can be explained by genetic drift. R2d2 is also associated with significantly reduced litter sizes in heterozygous mothers, making it a true selfish allele. Our data provide direct evidence of populations actively undergoing selfish sweeps, and demonstrate that meiotic drive can rapidly alter the genomic landscape in favor of mutations with neutral or even negative effects on overall Darwinian fitness. Further study will reveal the incidence of selfish sweeps, and will elucidate the relative contributions of selfish genes, adaptation and genetic drift to evolution