Genome-Wide Patterns of Recombination, Nucleotide Diversity and Linkage Disequilibrium in Eucalyptus from High Density SNP Genotyping and Pooled Whole-Genome Resequencing

We used a combination of whole-genome pooled resequencing and high density SNP genotyping of 72 unrelated chromosomes from wild populations to report the first genome-wide examination of the landscape of population recombination (rho), nucleotide diversity (theta_w) and linkage disequilibrium (r²) in Eucalyptus grandis. These are key genomic features that have profound impact on the understanding of fundamental evolutionary issues and on the practice of molecular breeding. Additionally, we built the two highest density linkage maps for Eucalyptus with >8,000 SNPs, resulting in a genome-wide recombination rate of ≈2.6 cM/Mb, offering further evidence for the completeness of the recently published Eucalyptus grandis genome sequence and providing an improved map framework to correct, in future genome updates, the few localized assembly inconsistencies that were observed in the current version 1.1. By genotyping 36K SNPs at variable distance intervals from 30 bp to several Mb, across coding and non-coding genomic regions, short and long range LD was captured, showing that r² fell to half its initial value within 3 kb and dropped to <0.2 within 5-7 kb, likely a reflection of variable effective population size histories and uneven rates of recombination across the genome. Coalescent-based estimates of rho derived from 4.7M million sequence-based SNPs and 36K chip-genotyped SNPs converged to the same population recombination rate ≈0.0005, leading to lower than expected estimates of effective population sizes (N_e ≈5,700-5,900) for E. grandis, possibly reflecting the reported Pleistocene-Holocene population bottlenecks and expansions. Eucalyptus displays one of the highest genome-wide nucleotide diversities in plants (theta_w = 0.0168), consistent with its exceptional phenotypic plasticity, revealing that mutation is more important than recombination in shaping the extant diversity in Eucalyptus (rho/theta_w = 0.03). The considerably slower decay of LD when assessed at the genome-wide scale, when compared to the previous reports based on the analysis of limited sequence stretches in a few candidate genes, indicates brighter prospects for GWAS in natural populations and substantiates the recent positive results of genomic selection in eucalypt breeding.