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

Abstract

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.

Multiple forms of selection shape reproductive isolation in a primate hybrid zone

“…In manakins (Parchman et al, ) and lycaenid butterflies (Gompert, Lucas, et al, ), loci with non‐neutral introgression also showed elevated differentiation in parental populations compared to neutral markers. In the house mouse hybrid zone, Janoušek et al () also observed higher differentiation for markers with reduced introgression, but contrary to our findings, loci with increased introgression showed lower differentiation compared to neutral markers. These results are consistent with the hypothesis that reproductive isolation arises as a by‐product of selection in allopatry, although we recognize that locus‐specific differentiation and introgression are determined by the complex interaction of many factors and that disentangling the effects of selection from other processes can be challenging (Beaumont & Balding, ; Gompert, Parchman, & Buerkle, ).…”

“…Similarly, we observed neutral and increased introgression for markers with very high, moderate and no differentiation (i.e., from F ST = 0 to F ST = 1) (Figure b). These observations are similar to those in other hybrid zones (e.g., Janoušek et al, , Schield et al, ) and are likely a reflection of the complexity of the interaction between selection, drift and recombination and suggest that these forces vary across the genome. Despite the mechanism of divergence, this also demonstrates that high differentiation in allopatry is not a perfect predictor for reproductive isolation.…”

Mammalian Meiotic Recombination: A Toolbox for Genome Evolution

“…On the one hand, genome reshuffling influences recombination landscapes. On the other hand, gene incompatibilities, reduced introgression, and higher differentiation are often associated with genomic regions with reduced recombination [Geraldes et al, 2011;Seehausen et al, 2014;Janoušek et al, 2015]. Speciation genes have been described mostly in Drosophila , including, for instance, Odysseus-site homeobox (OdsH) [Ting et al, 1998], JYalpha [Masly et al, 2006], and Overdrive (Ovd) genes [Phadnis and Orr, 2009].…”

Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates

“…This dramatic difference in the localization of hotspots and their evolutionary dynamics has important evolutionary consequences for genome structure and base composition, for linkage disequilibrium (LD) levels along the genome, as well as for introgression patterns in naturally occurring hybrids (Fullerton et al, 2001; McVean et al, 2004; Duret and Galtier, 2009; Janoušek et al, 2015). It is therefore important to establish the generality of these two mechanisms and characterize their distribution across species.…”