Assessing Multilocus Introgression Patterns: A Case Study on the Mouse X Chromosome in Central Europe

Macholán, Miloš; Baird, Stuart J. E.; Dufková, Petra; Munclinger, Pavel; Bímová, Barbora Vošlajerová; Piálek, Jaroslav

doi:10.1111/j.1558-5646.2011.01228.x

Cited by 114 publications

(118 citation statements)

References 98 publications

(172 reference statements)

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“…To fit cline shape and position consistently for an unknown selection regime, a "concordance" method was developed by Szymura and Barton (1986) and used to analyze the hybrid zones in Bombina and, most recently, used for the hybrid zone in Mus by Macholán et al (2011). This method is similar to the one in Gompert and Buerkle (2009), which uses diploid genotype frequencies.…”

Section: Discussionmentioning

confidence: 99%

Genetic Drift Widens the Expected Cline but Narrows the Expected Cline Width

Polechová

Barton

2011

Genetics

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Random genetic drift shifts clines in space, alters their width, and distorts their shape. Such random fluctuations complicate inferences from cline width and position. Notably, the effect of genetic drift on the expected shape of the cline is opposite to the naive (but quite common) misinterpretation of classic results on the expected cline. While random drift on average broadens the overall cline in expected allele frequency, it narrows the width of any particular cline. The opposing effects arise because locally, drift drives alleles to fixation-but fluctuations in position widen the expected cline. The effect of genetic drift can be predicted from standardized variance in allele frequencies, averaged across the habitat: hF i. A cline maintained by spatially varying selection (step change) is expected to be narrower by a factor of ffiffiffiffiffiffiffiffiffiffiffiffiffi 12hFi p relative to the cline in the absence of drift. The expected cline is broader by the inverse of this factor. In a tension zone maintained by underdominance, the expected cline width is narrower by about 1 -hF i relative to the width in the absence of drift. Individual clines can differ substantially from the expectation, and we give quantitative predictions for the variance in cline position and width. The predictions apply to clines in almost one-dimensional circumstances such as hybrid zones in rivers, deep valleys, or along a coast line and give a guide to what patterns to expect in two dimensions. WITHIN species, substantial genetic diversity may be maintained by the interaction between selection and gene flow. This may be manifest in gradients in heritable traits or in allele frequency (Endler 1977). Clines reflect the degradation by gene flow of adaptation to the local environment or genetic background, and they may be used to estimate the strength of selection experienced by natural populations. Often, it is assumed that the effects of drift on the realized clines can be neglected.Random genetic drift will shift clines from side to side, alter their width, and distort their shape (Felsenstein 1975;Slatkin and Maruyama 1975;Nagylaki 1978). Such random fluctuations complicate inferences from cline width and position, but may themselves be used to infer rates of gene flow, drift, and selection. More important, drift is expected to reduce local diversity and so to make selection less effective, thereby interfering with adaptation to local conditions. The common view is that genetic drift makes clines slightly shallower, because selection becomes less effective. This comes from a "generalization" of the effect of genetic drift on the "expected cline" as derived by Slatkin and Maruyama (1975) (see, e.g., Alleaume-Benharira et al. 2006). However, the characteristics of the expected cline do not necessarily give an adequate idea of the patterns we expect to see in specific clines. Here, we define the expected cline as the average allele frequency across independent realizations, taken at the same time, and so it includes the i...

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Section: Discussionmentioning

confidence: 99%

Genetic Drift Widens the Expected Cline but Narrows the Expected Cline Width

Polechová

Barton

2011

Genetics

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“…Moreover, tests of geographical concordance and coincidence among genetic or phenotypic clines can detect variable introgression and have been used to identify loci potentially associated with reproductive isolation [19][20][21]. Genomic clines are mathematical functions that describe the probability of locus-specific ancestry along a gradient in genomewide admixture or hybrid index, which is defined as the proportion of an admixed individual's genome inherited from one of two parental populations [12,22,23], with related models in earlier studies [15,[24][25][26]. This is not a spatial gradient, rather nearly pure individuals of each parental type occupy opposite ends of the gradient.…”

Section: Introductionmentioning

confidence: 99%

Genomics of isolation in hybrids

Gompert

Parchman

Buerkle

2012

Phil. Trans. R. Soc. B

124

240

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Hybrid zones are common in nature and can offer critical insights into the dynamics and components of reproductive isolation. Hybrids between diverged lineages are particularly informative about the genetic architecture of reproductive isolation, because introgression in an admixed population is a direct measure of isolation. In this paper, we combine simulations and a new statistical model to determine the extent to which different genetic architectures of isolation leave different signatures on genome-level patterns of introgression. We found that reproductive isolation caused by one or several loci of large effect caused greater heterogeneity in patterns of introgression than architectures involving many loci with small fitness effects, particularly when isolating factors were closely linked. The same conditions that led to heterogeneous introgression often resulted in a reasonable correspondence between outlier loci and the genetic loci that contributed to isolation. However, demographic conditions affected both of these results, highlighting potential limitations to the study of the speciation genomics. Further progress in understanding the genomics of speciation will require large-scale empirical studies of introgression in hybrid zones and model-based analyses, as well as more comprehensive modelling of the expected levels of isolation with different demographies and genetic architectures of isolation.

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“…QTLs for reduced testis weight were detected in the pseudoautosomal region and on chromosomes 2 and 4 (White et al, 2012). The pseudoautosomal region has been previously linked to meiotic arrest and F1 sterility in crosses between M. spretus and C57BL/6J (Guénet et al, 1990;Matsuda et al, 1991Matsuda et al, , 1992Hale et al, 1993 (Tucker et al, 1992;Payseur et al, 2004;Teeter et al, 2008;Macholan et al, 2011;Janoušek et al, 2012). This implies that the X chromosome is prominently involved in the establishment of reproductive isolation between the mouse subspecies in nature.…”

Section: The Large X Effect On Hybrid Sterilitymentioning

confidence: 78%

“…Haldane's rule infers the involvement of the sex chromosomes in hybrid sterility. Indeed, many quantitative trait loci (QTLs) for hybrid male sterility in mice were mapped on the X chromosome (Oka et al, 2004;Storchová et al, 2004;Good et al, 2008;White et al, 2011;Oka and Shiroishi, 2012), and limited gene flow on the X chromosome was observed between adjacent species or subspecies in natural hybrid zones (Tucker et al, 1992;Payseur et al, 2004;Teeter et al, 2008;Macholan et al, 2011;Janoušek et al, 2012). Such a disproportionate effect of X-linked loci on interspecific or intersubspecific hybrid fitness is called as "the large X effect" (Coyne and Orr, 1989).…”

Section: Introductionmentioning

confidence: 99%

Regulatory divergence of X-linked genes and hybrid male sterility in mice

Oka

Shiroishi

2014

Genes Genet. Syst.

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Postzygotic reproductive isolation is the reduction of fertility or viability in hybrids between genetically diverged populations. One example of reproductive isolation, hybrid male sterility, may be caused by genetic incompatibility between diverged genetic factors in two distinct populations. Genetic factors involved in hybrid male sterility are disproportionately located on the X chromosome. Recent studies showing the evolutionary divergence in gene regulatory networks or epigenetic effects suggest that the genetic incompatibilities occur at much broader levels than had previously been thought (e.g., incompatibility of protein-protein interactions). The latest studies suggest that evolutionary divergence of transcriptional regulation causes genetic incompatibilities in hybrid animals, and that such incompatibilities preferentially involve X-linked genes. In this review, we focus on recent progress in understanding hybrid sterility in mice, including our studies, and we discuss the evolutionary significance of regulatory divergence for speciation.

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Assessing Multilocus Introgression Patterns: A Case Study on the Mouse X Chromosome in Central Europe

Abstract: patibilities between interacting loci, the Bateson-DobzhanskyMuller model

Cited by 114 publications

References 98 publications

Genetic Drift Widens the Expected Cline but Narrows the Expected Cline Width

Genetic Drift Widens the Expected Cline but Narrows the Expected Cline Width

Genomics of isolation in hybrids

Regulatory divergence of X-linked genes and hybrid male sterility in mice

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