Patterns of cyto-nuclear linkage disequilibrium in Silene latifolia: genomic heterogeneity and temporal stability

Abstract

Non-random association of alleles in the nucleus and cytoplasmic organelles, or cyto-nuclear linkage disequilibrium (LD), is both an important component of a number of evolutionary processes and a statistical indicator of others. The evolutionary significance of cyto-nuclear LD will depend on both its magnitude and how stable those associations are through time. Here, we use a longitudinal population genetic data set to explore the magnitude and temporal dynamics of cyto-nuclear disequilibria through time. We genotyped 135 and 170 individuals from 16 and 17 patches of the plant species Silene latifolia in Southwestern VA, sampled in 1993 and 2008, respectively. Individuals were genotyped at 14 highly polymorphic microsatellite markers and a single-nucleotide polymorphism (SNP) in the mitochondrial gene, atp1. Normalized LD (D') between nuclear and cytoplasmic loci varied considerably depending on which nuclear locus was considered (ranging from 0.005-0.632). Four of the 14 cyto-nuclear associations showed a statistically significant shift over approximately seven generations. However, the overall magnitude of this disequilibrium was largely stable over time. The observed origin and stability of cyto-nuclear LD is most likely caused by the slow admixture between anciently diverged lineages within the species' newly invaded range, and the local spatial structure and metapopulation dynamics that are known to structure genetic variation in this system.

Figure 1

Standardized cyto-nuclear LD (D′) between 14 nuclear loci and a SNP in the mitochondrial gene atp1 found in populations of S. latifolia sampled in 1993 and 2008 with a well-characterized metapopulation located in Giles County, VA, USA. Values of D′ can range from –1.0 to 1.0. Within the sampled plant populations, D′ was found to range from –0.424 to 0.6211 in 1993 and –0.6316 to 0.3888 in 2008. There was a general trend for an overall decrease in D′ between sampling periods, though only slat85 showed a significant (positive) change in overall cyto-nuclear D′ based upon our t-test of samples (*P<0.05 after Benjamini–Hochberg correction). slat33, slat72 and SL_eSSR20 all showed a significant decrease in D′.