Genome‐wide architecture of reproductive isolation in a naturally occurring hybrid zone between<i>Mus musculus musculus</i>and<i>M. m. domesticus</i>

Janoušek, Václav; Wang, Liuyang; Luzynski, Ken; Dufková, Petra; Vyskočilová, Martina; Nachman, Michael W.; Munclinger, Pavel; Macholán, Miloš; Piálek, Jaroslav; Tucker, Priscilla K.

doi:10.1111/j.1365-294x.2012.05583.x

Cited by 149 publications

(157 citation statements)

References 108 publications

(175 reference statements)

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“…Indeed, there are other evolutionary mechanisms that could explain extended LD patterns (such as segregating chromosomal rearrangements, Rieseberg, 2001;Hoffman and Rieseberg, 2008; or epistatic selection linked to post-zygotic reproductive barriers, Coyne and Orr, 2004;Presgraves, 2010;Janoušek et al, 2012 and so on), but all of them are speculative in relation to our data. Consequently, we prefer to leave this question open.…”

Section: Confounding Effects On Neutrality Testingmentioning

confidence: 50%

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

et al. 2014

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We analyzed the genetic mosaic of speciation in two hybridizing Mediterranean white oaks from the Iberian Peninsula (Quercus faginea Lamb. and Quercus pyrenaica Willd.). The two species show ecological divergence in flowering phenology, leaf morphology and composition, and in their basic or acidic soil preferences. Ninety expressed sequence tag-simple sequence repeats (EST-SSRs) and eight nuclear SSRs were genotyped in 96 trees from each species. Genotyping was designed in two steps. First, we used 69 markers evenly distributed over the 12 linkage groups (LGs) of the oak linkage map to confirm the species genetic identity of the sampled genotypes, and searched for differentiation outliers. Then, we genotyped 29 additional markers from the chromosome bins containing the outliers and repeated the multilocus scans. We found one or two additional outliers within four saturated bins, thus confirming that outliers are organized into clusters. Linkage disequilibrium (LD) was extensive; even for loosely linked and for independent markers. Consequently, score tests for association between two-marker haplotypes and the 'species trait' showed a broad genomic divergence, although substantial variation across the genome and within LGs was also observed. We discuss the influence of several confounding effects on neutrality tests and review the evolutionary processes leading to extensive LD. Finally, we examine how LD analyses within regions that contain outlier clusters and quantitative trait loci can help to identify regions of divergence and/or genomic hitchhiking in the light of predictions from ecological speciation theory.

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Section: Confounding Effects On Neutrality Testingmentioning

confidence: 50%

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

et al. 2014

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“…This problem plagues most genetic studies of reproductive isolation and is difficult to dismiss. But several lines of evidence suggest the QTL we found contribute to hybrid incompatibilities, including their involvement in X-autosome epistatic interactions , their overlap with regions of low introgression in the European hybrid zone (Janoušek et al 2012), and their colocalization with trans-expression-QTL hotspots mapped in hybrids (Turner et al 2014). Finally, we assumed that overlapping QTL from the two crosses reflect the same genetic changes.…”

Section: Discussionmentioning

confidence: 99%

The Pace of Hybrid Incompatibility Evolution in House Mice

2015

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Hybrids between species are often sterile or inviable. This form of reproductive isolation is thought to evolve via the accumulation of mutations that interact to reduce fitness when combined in hybrids. Mathematical formulations of this "DobzhanskyMuller model" predict an accelerating buildup of hybrid incompatibilities with divergence time (the "snowball effect"). Although the Dobzhansky-Muller model is widely accepted, the snowball effect has only been tested in two species groups. We evaluated evidence for the snowball effect in the evolution of hybrid male sterility among subspecies of house mice, a recently diverged group that shows partial reproductive isolation. We compared the history of subspecies divergence with patterns of quantitative trait loci (QTL) detected in F 2 intercrosses between two pairs of subspecies (Mus musculus domesticus with M. m. musculus and M. m. domesticus with M. m. castaneus). We used a recently developed phylogenetic comparative method to statistically measure the fit of these data to the snowball prediction. To apply this method, QTL were partitioned as either shared or unshared in the two crosses. A heuristic partitioning based on the overlap of QTL confidence intervals produced unambiguous support for the snowball effect. An alternative approach combining data among crosses favored the snowball effect for the autosomes, but a linear accumulation of incompatibilities for the X chromosome. Reasoning that the X chromosome analyses are complicated by low mapping resolution, we conclude that hybrid male sterility loci have snowballed in house mice. Our study illustrates the power of comparative genetic mapping for understanding mechanisms of speciation.

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“…However, there are published QTL mapping results for the other two pairwise comparisons (White et al , 2012 and many studies of the hybrid zone between M. m. domesticus and M. m. musculus (e.g., Vanlerberghe et al 1986Vanlerberghe et al , 1988Tucker et al 1992;Prager et al 1993;Munclinger et al 2002; Macholan et al 2007;Teeter et al 2008Teeter et al , 2010Janoušek et al 2012). For QTL, we identified overlap between 1.5-LOD intervals associated with sterility phenotypes and highly differentiated regions in the window analysis based on all SNPs (White et al , 2012.…”

Section: Identifying Candidate Regions For Reproductive Isolationmentioning

confidence: 95%

“…The overlap between differentially expressed genes and candidate BDMIs loci from the hyrbid zone study of Janoušek et al (2012) was also not more than expected by chance. However, the overlap between highly differentiated regions and the candidate BDMI loci ranks in the 92nd percentile of simulated data (Janoušek et al 2012). Regions of overlap between all three kinds of studies (QTL, candidate BDMI loci from the hybrid zone, and regions of high differentiation) are particularly promising candidates for reproductive isolation.…”

Section: Testis-specific Expressionmentioning

confidence: 99%

Genome-Wide Patterns of Differentiation Among House Mouse Subspecies

2014

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One approach to understanding the genetic basis of speciation is to scan the genomes of recently diverged taxa to identify highly differentiated regions. The house mouse, Mus musculus, provides a useful system for the study of speciation. Three subspecies (M. m. castaneus, M. m. domesticus, and M. m. musculus) diverged 350 KYA, are distributed parapatrically, show varying degrees of reproductive isolation in laboratory crosses, and hybridize in nature. We sequenced the testes transcriptomes of multiple wild-derived inbred lines from each subspecies to identify highly differentiated regions of the genome, to identify genes showing high expression divergence, and to compare patterns of differentiation among subspecies that have different demographic histories and exhibit different levels of reproductive isolation. Using a sliding-window approach, we found many genomic regions with high levels of sequence differentiation in each of the pairwise comparisons among subspecies. In all comparisons, the X chromosome was more highly differentiated than the autosomes. Sequence differentiation and expression divergence were greater in the M. m. domesticus-M. m. musculus comparison than in either pairwise comparison with M. m. castaneus, which is consistent with laboratory crosses that show the greatest reproductive isolation between M. m. domesticus and M. m. musculus. Coalescent simulations suggest that differences in estimates of effective population size can account for many of the observed patterns. However, there was an excess of highly differentiated regions relative to simulated distributions under a wide range of demographic scenarios. Overlap of some highly differentiated regions with previous results from QTL mapping and hybrid zone studies points to promising candidate regions for reproductive isolation. U NDERSTANDING the genetic basis of speciation is a fundamental goal of evolutionary biology. This problem has primarily been approached in two ways: through laboratory studies using crosses and through studies of genetic variation in natural populations. Laboratory studies control for genetic background and environment, and they make it possible to connect genotype and phenotype. These types of studies have produced some spectacular successes including the identification of individual genes underlying postzygotic isolation in Drosophila (e.g., Ting et al. 1998;Presgraves et al. 2003;Brideau et al. 2006;Masly et al. 2006), Arabidopsis (Bomblies et al. 2007;Bikard et al. 2009), Mus (Mihola et al. 2009), and others (reviewed in Presgraves 2010 and Nosil and Schluter 2011).Studies of natural populations rely on the idea that regions of the genome that are important in reproductive isolation may be more differentiated than other regions of the genome. Therefore, by studying patterns of differentiation, one may gain insight into the genomic regions that underlie isolation. The idea that the genomes of closely related species are mosaics of differentiated and less differentiated regions is not new and first e...

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Genome‐wide architecture of reproductive isolation in a naturally occurring hybrid zone betweenMus musculus musculusandM. m. domesticus

Cited by 149 publications

References 108 publications

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

The Pace of Hybrid Incompatibility Evolution in House Mice

Genome-Wide Patterns of Differentiation Among House Mouse Subspecies

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