The Contribution of Epigenetics to Evolutionary Adaptation in Zingiber kawagoii Hayata (Zingiberaceae) Endemic to Taiwan

We epigenotyped 211 individuals from 17 Zingiber kawagoii populations using methylation-sensitive amplification polymorphism (MSAP) and investigated the associations of methylated (mMSAP) and unmethylated (uMSAP) loci with 16 environmental variables. Data regarding genetic variation based on amplified fragment length polymorphism (AFLP) were obtained from an earlier study. We found a significant positive correlation between genetic and epigenetic variation. Significantly higher mean mMSAP and uMSAP uH(E) (unbiased expected heterozygosity: 0.223 and 0.131, respectively, p < 0.001) per locus than that estimated based on AFLP (uH(E) = 0.104) were found. Genome scans detected 10 mMSAP and 9 uMSAP F-ST outliers associated with various environmental variables. A significant linear fit for 11 and 12 environmental variables with outlier mMSAP and uMSAP ordination, respectively, generated using full model redundancy analysis (RDA) was found. When conditioned on geography, partial RDA revealed that five and six environmental variables, respectively, were the most important variables influencing outlier mMSAP and uMSAP variation. We found higher genetic (average F-ST = 0.298) than epigenetic (mMSAP and uMSAP average F-ST = 0.044 and 0.106, respectively) differentiation and higher genetic isolation-by-distance (IBD) than epigenetic IBD. Strong epigenetic isolation-by-environment (IBE) was found, particularly based on the outlier data, controlling either for geography (mMSAP and uMSAP b(E) = 0.128 and 0.132, respectively, p = 0.001) or for genetic structure (mMSAP and uMSAP b(E) = 0.105 and 0.136, respectively, p = 0.001). Our results suggest that epigenetic variants can be substrates for natural selection linked to environmental variables and complement genetic changes in the adaptive evolution of Z. kawagoii populations.

Automated summary

In this study, we examined the associations between genetic and epigenetic variation in Zingiber kawagoii populations. We found a significant positive correlation between the two. Genome scans identified several outlier loci associated with different environmental variables. Additionally, both geography and genetic structure were found to influence the variation in epigenetic markers.