Katherine C. Teeter

THE VARIABLE GENOMIC ARCHITECTURE OF ISOLATION BETWEEN HYBRIDIZING SPECIES OF HOUSE MICE

Studies of the genetics of hybrid zones can provide insight into the genomic architecture of species boundaries. By examining patterns of introgression of multiple loci across a hybrid zone, it may be possible to identify regions of the genome that have experienced selection. Here, we present a comparison of introgression in two replicate transects through the house mouse hybrid zone through central Europe, using data from 41 single nucleotide markers. Using both genomic and geographic clines, we found many differences in patterns of introgression between the two transects, as well as some similarities. We found that many loci may have experienced the effects of selection at linked sites, including selection against hybrid genotypes, as well as positive selection in the form of genotypes introgressed into a foreign genetic background. We also found many positive associations of conspecific alleles among unlinked markers, which could be caused by epistatic interactions. Different patterns of introgression in the two transects highlight the challenge of using hybrid zones to identify genes underlying isolation and raise the possibility that the genetic basis of isolation between these species may be dependent on the local population genetic make‐up or the local ecological setting.

Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone

Theory predicts that naturally occurring hybrid zones between genetically distinct taxa can move over space and time as a result of selection and/or demographic processes, with certain types of hybrid zones being more or less likely to move. Determining whether a hybrid zone is stationary or moving has important implications for understanding evolutionary processes affecting interactions in hybrid populations. However, direct observations of hybrid zone movement are difficult to make unless the zone is moving rapidly. Here, evidence for movement in the house mouse Mus musculus domesticus × Mus musculus musculus hybrid zone is provided using measures of LD and haplotype structure among neighbouring SNP markers from across the genome. Local populations of mice across two transects in Germany and the Czech Republic were sampled, and a total of 1301 mice were genotyped at 1401 markers from the nuclear genome. Empirical measures of LD provide evidence for extinction and (re)colonization in single populations and, together with simulations, suggest hybrid zone movement because of either geography‐dependent asymmetrical dispersal or selection favouring one subspecies over the other.

Haplotype dimorphism in a SNP collection from Drosophila melanogaster

A moderate resolution single nucleotide polymorphism (SNP) map of the genome of Drosophila melanogaster that is designed for use in quantitative genetic mapping is described. Seventeen approximately 500 nucleotide gene sequences spaced at 10 to 20 centimorgan intervals were combined with 49 shorter sequence tag sites (STSs) at 5 to 10 centimorgan intervals to generate a map that should not leave any gaps greater than one half of a chromosome arm when any two wild type lines are compared. Of 20 markers with sufficient polymorphism to construct haplotype cladograms, 13 showed evidence for two divergent classes of haplotype. The possible mechanisms for and implications of the unexpected finding that two thirds of all short gene sequences in D. melanogaster may be dimorphic are discussed, including the suggestion that admixture between two separate lineages may have been a major event in the history of the species.

Functional Organization of the Genome May Shape the Species Boundary in the House Mouse

Genomic features such as rate of recombination and differentiation have been suggested to play a role in species divergence. However, the relationship of these phenomena to functional organization of the genome in the context of reproductive isolation remains unexplored. Here, we examine genomic characteristics of the species boundaries between two house mouse subspecies (Mus musculus musculus/M. m. domesticus). These taxa form a narrow semipermeable zone of secondary contact across Central Europe. Due to the incomplete nature of reproductive isolation, gene flow in the zone varies across the genome. We present an analysis of genomic differentiation, rate of recombination, and functional composition of genes relative to varying amounts of introgression. We assessed introgression using 1,316 autosomal single nucleotide polymorphism markers, previously genotyped in hybrid populations from three transects. We found a significant relationship between amounts of introgression and both genomic differentiation and rate of recombination with genomic regions of reduced introgression associated with higher genomic differentiation and lower rates of recombination, and the opposite for genomic regions of extensive introgression. We also found a striking functional polarization of genes based on where they are expressed in the cell. Regions of elevated introgression exhibit a disproportionate number of genes involved in signal transduction functioning at the cell periphery, among which olfactory receptor genes were found to be the most prominent group. Conversely, genes expressed intracellularly and involved in DNA binding were the most prevalent in regions of reduced introgression. We hypothesize that functional organization of the genome is an important driver of species divergence.

Linkage disequilibrium approaches for detecting hybrid zone movement

In a series of papers spanning over a decade (e.g. Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985, 1989), Barton and Hewitt explored the nature of hybrid zones that are formed when genetically distinct populations overlap and reproduce (Barton and Hewitt, 1985, 1989). They viewed most hybrid zones as ‘tension zones’ (Key, 1968), i.e. clines maintained by a balance between dispersal and selection against hybrids, and they proposed that tension zones can be stationary or they can move across geographic space due to demographic differences between populations or as a result of asymmetric selection (Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985). Determining whether a hybrid zone is stationary or moving has important implications for understanding the evolutionary processes affecting interactions in hybrid populations. However, in a recent review of the hybrid zone literature, Buggs (2007) discussed the difficulties in detecting hybrid zone movement, especially from patterns of gene flow. For example, although a moving tension zone will leave a signature tail of neutral clines in its wake (Arntzen and Wallis, 1991), this pattern could also be interpreted as the adaptive introgression of alleles away from a stationary front. Buggs (2007) concluded that evidence for moving hybrid zones was not well established in the literature. The well-studied hybrid zone between genetically distinct populations of house mice,Mus musculus musculus andM. m. domesticus (also referred to in the literature asMus musculus andMus domesticus) (Hunt and Selander, 1973; Sage et al., 1986b; Vanlerberghe et al., 1986, 1988a, b; Tucker et al., 1992; Fel-Clair et al., 1996; Orth et al., 1996; Boissinot and Boursot, 1997; Prager et al., 1997; Munclinger et al., 2002;

Evolution of the House Mouse: Linkage disequilibrium approaches for detecting hybrid zone movement

In a series of papers spanning over a decade (e.g. Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985, 1989), Barton and Hewitt explored the nature of hybrid zones that are formed when genetically distinct populations overlap and reproduce (Barton and Hewitt, 1985, 1989). They viewed most hybrid zones as ‘tension zones’ (Key, 1968), i.e. clines maintained by a balance between dispersal and selection against hybrids, and they proposed that tension zones can be stationary or they can move across geographic space due to demographic differences between populations or as a result of asymmetric selection (Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985). Determining whether a hybrid zone is stationary or moving has important implications for understanding the evolutionary processes affecting interactions in hybrid populations. However, in a recent review of the hybrid zone literature, Buggs (2007) discussed the difficulties in detecting hybrid zone movement, especially from patterns of gene flow. For example, although a moving tension zone will leave a signature tail of neutral clines in its wake (Arntzen and Wallis, 1991), this pattern could also be interpreted as the adaptive introgression of alleles away from a stationary front. Buggs (2007) concluded that evidence for moving hybrid zones was not well established in the literature. The well-studied hybrid zone between genetically distinct populations of house mice,Mus musculus musculus andM. m. domesticus (also referred to in the literature asMus musculus andMus domesticus) (Hunt and Selander, 1973; Sage et al., 1986b; Vanlerberghe et al., 1986, 1988a, b; Tucker et al., 1992; Fel-Clair et al., 1996; Orth et al., 1996; Boissinot and Boursot, 1997; Prager et al., 1997; Munclinger et al., 2002;

Linkage disequilibrium approaches for detecting hybrid zone movement: A study of the house mouse hybrid zone in southern bavaria

In a series of papers spanning over a decade (e.g. Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985, 1989), Barton and Hewitt explored the nature of hybrid zones that are formed when genetically distinct populations overlap and reproduce (Barton and Hewitt, 1985, 1989). They viewed most hybrid zones as ‘tension zones’ (Key, 1968), i.e. clines maintained by a balance between dispersal and selection against hybrids, and they proposed that tension zones can be stationary or they can move across geographic space due to demographic differences between populations or as a result of asymmetric selection (Hewitt, 1975; Barton, 1979; Barton and Hewitt, 1985). Determining whether a hybrid zone is stationary or moving has important implications for understanding the evolutionary processes affecting interactions in hybrid populations. However, in a recent review of the hybrid zone literature, Buggs (2007) discussed the difficulties in detecting hybrid zone movement, especially from patterns of gene flow. For example, although a moving tension zone will leave a signature tail of neutral clines in its wake (Arntzen and Wallis, 1991), this pattern could also be interpreted as the adaptive introgression of alleles away from a stationary front. Buggs (2007) concluded that evidence for moving hybrid zones was not well established in the literature. The well-studied hybrid zone between genetically distinct populations of house mice,Mus musculus musculus andM. m. domesticus (also referred to in the literature asMus musculus andMus domesticus) (Hunt and Selander, 1973; Sage et al., 1986b; Vanlerberghe et al., 1986, 1988a, b; Tucker et al., 1992; Fel-Clair et al., 1996; Orth et al., 1996; Boissinot and Boursot, 1997; Prager et al., 1997; Munclinger et al., 2002;