Evolution of Zygotic Linkage Disequilibrium in a Finite Local Population

Abstract

One crucial feature of zygotic linkage disequilibrium (LD) analysis is its direct use of diploid genotyping data, irrespective of the type of mating system. Previous theories from an evolutionary perspective mainly focus on gametic LD, but the equivalent development for zygotic LD is not available. Here I study the evolution of zygotic LD and the covariances between gametic and zygotic LDs or between distinct zygotic LDs in a finite local population under constant immigration from a continent population. I derive the analytical theory under genetic hitchhiking effects or in a neutral process. Results indicate that zygotic LDs (diploid level) are more informative than gametic LD (haploid level) in indicating the effects of different evolutionary forces. Zygotic LDs may be greater than or comparable to gametic LD under the epistatic selection process, but smaller than gametic LD under the non epistatic selection process. The covariances between gametic and zygotic LDs are strongly affected by the mating system, linkage distance, and genetic drift effects, but weakly affected by seed and pollen flow and natural selection. The covariances between different zygotic LDs are generally robust to the effects of gene flow, selection, and linkage distance, but sensitive to the effects of genetic drift and mating system. Consistent patterns exist for the covariances between the zygotic LDs for the two-locus genotypes with one common genotype at one locus or without any common genotype at each locus. The results highlight that zygotic LDs can be applied to detecting natural population history.

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

“…These two levels of LDs are genetically related, but gametic LD contains the compounded information of epistatic selection from both stages. Zygotic LD is mainly associated with the epistasis in the diploid zygotic stage [ 15 ].…”

“…The difference is that these processes mainly generate statistical non-random associations between loci, different from the effects of epistatic selection that generates functional non-random associations. 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. Recently, Hu [ 15 ] has showed that zygotic LDs, owning to their diverse patterns under distinct evolutionary processes among two-locus genotypes, are more informative than the commonly used gametic LD in revealing natural population history. In Homo sapiens species, gametic LD has been extensively investigated in many populations of different origins, and its pattern is applied for different purposes, such as mapping single nucleotide polymorphisms (SNPs) for causal diseases and examining population demography [ 22 , 23 ].…”

Assessing Postzygotic Isolation Using Zygotic Disequilibria in Natural Hybrid Zones

“…Previous studies of zygotic LD lie in the aspects of the effects of partial inbreeding [24] or a mixed mating system [25], the proposition of testing selection in an artificial population [18], [19], the relevant conceptual insights [26], [27], the statistical issue on estimating zygotic LD [22], [23], [28], the potential application of zygotic LD to mapping quantitative trait loci (QTL; [29]), and the discussions of zygotic LDs for elucidating evolutionary processes [30], [31]. Hu [32] further shows that zygotic LD is more informative than gametic LD in detecting natural population history in a continent-island model. So far, this measure has not been applied to detecting the genetic mechanisms of reproductive isolation in hybrid zones except the use of cytonuclear genotypic LD, a conceptual analogy to zygotic LD [33], [34].…”

A unifying experimental design for dissecting tree genomes

“…Zygotic disequilibria, defined as non-random associations of genotypes at different loci [19][20][21], do not rely on the assumption of HWE, and have been thought to be powerful tools for population genetic studies [22,23]. A full definition of zygotic disequilibria includes non-random associations at individual loci, within and between gametes, between a zygote and a gamete at different loci, and between zygotes at different loci [21].…”