Assessing Postzygotic Isolation Using Zygotic Disequilibria in Natural Hybrid Zones

Abstract

Hybrid zones as windows on evolutionary processes provide a natural laboratory for studying the genetic basis and mechanisms of postzygotic isolation. One resultant pattern in hybrid zones is the Hardy-Weinberg disequilibrium (HWD) for a single locus or the linkage disequilibrium (LD) for multiple loci produced by natural selection against hybrids. However, HWD and the commonly used low-order gametic or composite digenic LD cannot fully reflect the pattern of the high-order genotypic interactions. Here we propose the use of zygotic LD to elucidate the selection mechanisms of postzygotic isolation, and its calculation is based on genotypic frequencies only, irrespective of the type of mating system. We numerically and analytically show that the maximum composite digenic LD is always greater than the maximum absolute zygotic LD under the linear-additive selection, but is comparable to or smaller than the maximum absolute zygotic LD under the strong epistatic selection. Selection mechanisms can be inferred by testing such differences. We analyze a previously reported mouse hybrid zone assayed with genome-wide SNPs, and confirm that the composite digenic LD cannot appropriately indicate all possible significant genotypic interactions for a given SNP pair. A large proportion of significant zygotic LDs, ∼75% in general in the mouse hybrid zone, cannot be revealed from the composite digenic LD analysis. Statistical tests indicate that epistatic selection occurred among multiple loci in the mouse hybrid zone. The results highlight that the joint patterns of the composite digenic and zygotic LDs can help to elucidate the selection mechanism that is potentially involved in postzygotic isolation.

Mating system as a barrier to gene flow

“…A constant proportion of pollen grains, m P /2, and seeds, m S /2, are exchanged between two adjacent neighbors for each population. The simulation procedure and algorithm are based on the life cycle of plants described in the preceding section and Appendix A, similar to the simulation of an ecological zone in Hu and Yeh (2014). Figure 1 shows the gene frequency clines in a hybrid zone at the 1000th generation under a fixed α 1 but different α 2 's.…”

Genomic Scans of Zygotic Disequilibrium and Epistatic SNPs in HapMap Phase III Populations

“…Although zygotic LD has long been conceptually appreciated [ 11 , 12 ], its statistical properties and evolutionary theory have not been extensively developed [ 13 , 14 , 15 ]. Practical analysis of zygotic LDs is mainly in crops for detecting selection [ 16 , 17 ], in dogs [ 18 ] and cattle [ 19 , 20 ] for characterizing population structure, and in a mouse hybrid zone for assessing postzygotic isolation [ 21 ]. The crucial difference between gametic and zygotic LDs lies in that zygotic LD calculation uses unphased genotypic data, different from gametic LD calculation that uses phased genotypic data.…”

“…Besides the utility of zygotic LDs for characterizing population history, Hu [ 15 ] and Hu and Yeh [ 21 ] further show that gametic and composite digenic LDs (low-order LD) are always greater than the maximum zygotic LD (high-order LD) in a population under the processes of migration, genetic drift, and additive selection. Only epistatic selection can produce a contrasting pattern, i.e.…”

“…The composite digenic LD is used to infer Dobzhansky-Muller incompatibility model in a natural mouse hybrid zone [ 26 ]. Here, we search for epistatic SNPs by testing the difference between the composite digenic and maximum zygotic LDs in human populations [ 15 , 21 ].…”

“…One is that the trait refers to the general fitness, not a specific complex disease that may affect fitness. The epistatic selection for fitness naturally occurs in a population [ 15 , 21 ], emphasizing the functional interaction between loci. The existing methods for detecting epistasis often work on specific traits, such as the approach of genome-wide association studies (GWAS) for specific complex diseases [ 27 ].…”