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 uHE (unbiased expected heterozygosity: 0.223 and 0.131, respectively, p < 0.001) per locus than that estimated based on AFLP (uHE = 0.104) were found. Genome scans detected 10 mMSAP and 9 uMSAP FST 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 FST = 0.298) than epigenetic (mMSAP and uMSAP average FST = 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 ßE = 0.128 and 0.132, respectively, p = 0.001) or for genetic structure (mMSAP and uMSAP ßE = 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.

Pattern of Adaptive Divergence in Zingiber kawagoii Hayata (Zingiberaceae) along a Narrow Latitudinal Range.

Ecological and evolutionary processes linking adaptation to environment are related to species' range shifts. In this study, we employed amplified-fragment-length-polymorphism-based genome scan methods to identify candidate loci among Zingiber kawagoii populations inhabiting varying environments distributed at low to middle elevations (143-1488 m) in a narrow latitudinal range (between 21.90 and 25.30° N). Here, we show evidence of selection driving the divergence of Z. kawagoii. Twenty-six FST outliers were detected, which were significantly correlated with various environmental variables. The allele frequencies of nine FST outliers were either positively or negatively correlated with the population mean FST. Using several independent approaches, we found environmental variables act in a combinatorial fashion, best explaining outlier genetic variation. Nonetheless, we found that adaptive divergence was affected mostly by annual temperature range, and it is significantly positively correlated with latitude and significantly negatively correlated with the population mean FST. This study addresses a latitudinal pattern of changes in annual temperature range (which ranged from 13.8 °C in the Lanyu population to 18.5 °C in the Wulai population) and emphasizes the pattern of latitudinal population divergence closely linked to the allele frequencies of adaptive loci, acting in a narrow latitudinal range. Our results also indicate environmentally dependent local adaptation for both leading- and trailing-edge populations.

Adaptive Divergence without Distinct Species Relationships Indicate Early Stage Ecological Speciation in Species of the Rhododendronpseudochrysanthum Complex Endemic to Taiwan.

The testing association of environmental variables with genetic and epigenetic variation could be crucial to deciphering the effects of environmental factors playing roles as selective drivers in ecological speciation. Although ecological speciation may occur in closely related species, species boundaries may not be established over a short evolutionary timescale. Here, we investigated the genetic and epigenetic variations using amplified fragment length polymorphism (AFLP) and methylation-sensitive amplification polymorphism (MSAP), respectively, and tested their associations with environmental variables in populations of four closely related species in the R. pseudochrysanthum complex. No distinctive species relationships were found using genetic clustering analyses, neighbor-joining tree, and neighbor-net tree based on the total AFLP variation, which is suggestive of the incomplete lineage sorting of ancestral variation. Nonetheless, strong isolation-by-environment and adaptive divergence were revealed, despite the significant isolation-by-distance. Annual mean temperature, elevation, normalized difference vegetation index, and annual total potential evapotranspiration were found to be the most important environmental variables explaining outlier genetic and epigenetic variations. Our results suggest that the four closely related species of the R. pseudochrysanthum complex share the polymorphism of their ancestor, but reproductive isolation due to ecological speciation can occur if local environmental divergence persists over time.

Testing the Effect of Mountain Ranges as a Physical Barrier to Current Gene Flow and Environmentally Dependent Adaptive Divergence in Cunninghamia konishii (Cupressaceae).

Populations can be genetically isolated by differences in their ecology or environment that hampered efficient migration, or they may be isolated solely by geographic distance. Moreover, mountain ranges across a species' distribution area might have acted as barriers to gene flow. Genetic variation was quantified using amplified fragment length polymorphism (AFLP) and 13 selective amplification primer combinations used generated a total of 482 fragments. Here, we tested the barrier effects of mountains on gene flow and environmentally dependent local adaptation of Cunninghamia konishii occur in Taiwan. A pattern of genetic isolation by distance was not found and variation partitioning revealed that environment explained a relatively larger proportion of genetic variation than geography. The effect of mountains as barriers to genetic exchange, despite low population differentiation indicating a high rate of gene flow, was found within the distribution range of C. konishii. Twelve AFLP loci were identified as potential selective outliers using genome-scan methods (BAYESCAN and DFDIST) and strongly associated with environmental variables using regression approaches (LFMM, Samßada, and rstanarm) demonstrating adaptive divergence underlying local adaptation. Annual mean temperature, annual precipitation, and slope could be the most important environmental factors causally associated with adaptive genetic variation in C. konishii. The study revealed the existence of physical barriers to current gene flow and environmentally dependent adaptive divergence, and a significant proportion of the rate of gene flow may represent a reflection of demographic history.

The Contribution of Neutral and Environmentally Dependent Processes in Driving Population and Lineage Divergence in Taiwania (Taiwania cryptomerioides).

The question of what determines divergence both between and within species has been the central topic in evolutionary biology. Neutral drift and environmentally dependent divergence are predicted to play roles in driving population and lineage divergence. However, neutral drift may preclude adaptation if the rate of gene flow between populations is high. Here, we sampled populations of three Taiwania (Taiwania cryptomerioides) lineages occurring in Taiwan, the mainland of China (Yunnan-Myanmar border), and northern Vietnam, and tested the relative strength of neutral drift and divergent selection in shaping divergence of those populations and lineages. We quantified genetic and epigenetic variation, respectively, using amplified fragment length polymorphism (AFLP) and methylation-sensitive amplification polymorphism (MSAP). Analysis of 1413 AFLP and 462 MSAP loci using frequency-based genome scan methods and generalized linear models (GLMs) found no potential selective outliers when only Taiwanese populations were examined, suggesting that neutral drift was the predominant evolutionary process driving differentiation between those populations. However, environmentally associated divergence was found when lineages were compared. Thirty-two potential selective outliers were identified based on genome scans and their associations with environmental variables were tested with GLMs, generalized linear mixed effect models (GLMMs), and model selection with a model averaging approach. Ten loci (six AFLP and four MSAP) were found to be strongly associated with environmental variables, particularly monthly temperature variation and normalized difference vegetation index (NDVI) using model selection and a model averaging approach. Because only a small portion of genetic and epigenetic loci were found to be potential selective outliers, neutral evolutionary process might also have played crucial roles in driving lineage divergence, particularly between geographically and genetically isolated island and mainland Asia lineages. Nevertheless, the vast amount of neutral drift causing genetic and epigenetic variations might have the potential for adaptation to future climate changes. These could be important for the survival of Taiwania in different geographic areas.