Abstract
Genetic diversity defines the evolutionary potential of a species, yet mounting evidence suggests that epigenetic diversity could also contribute to adaptation. Elucidating the complex interplay between genetic and epigenetic variation in wild populations remains a challenge for evolutionary biologists, and the intriguing possibility that epigenetic diversity could compensate for the loss of genetic diversity is one aspect that remains basically unexplored in wild plants. This hypothesis is addressed in this paper by comparing the extent and patterns of genetic and epigenetic diversity of phylogenetically closely related but ecologically disparate species. Seven pairs of congeneric species from Cazorla mountains in south-eastern Spain were studied, each pair consisting of one endemic, restricted-range species associated to stressful environments, and one widespread species occupying more favourable habitats. The prediction was tested that endemic species should have lower genetic diversity due to population fragmentation, and higher epigenetic diversity induced by environmental stress, than their widespread congeners. Genetic (DNA sequence variants) and epigenetic (DNA cytosine methylation variants) diversities and their possible co-variation were assessed in three populations of each focal species using amplified fragment length polymorphism (AFLP) and methylation-sensitive AFLP (MSAP). All species and populations exhibited moderate to high levels of genetic polymorphism irrespective of their ecological characteristics. Epigenetic diversity was greater than genetic diversity in all cases. Only in endemic species were the two variables positively related, but the difference between epigenetic and genetic diversity was greater at populations with low genetic polymorphism. Results revealed that the relationship between genetic and epigenetic diversity can be more complex than envisaged by the simple hypothesis addressed in this study, and highlight the need of additional research on the actual role of epigenetic variation as a source of phenotypic diversity before a realistic understanding of the evolutionary relevance of epigenetic phenomena in plant adaptation can be achieved.
Highlights
The genetic diversity of species and populations has multiple implications for their ecology, evolution and survival
Each pair consisted of one narrow endemic species with a restricted geographic distribution and that is a specialist of stressing Mediterranean microhabitats or that occurs only in highly specific habitats, and one species with a widespread geographic distribution which utilizes a broad range of habitat types
We investigated epigenetic diversity associated to changes in the methylation status of hundreds of Methyl Sensitive AFLP (MSAP) markers and compared it to genetic diversity estimates for roughly similar numbers of Amplified Fragment Length Polymorphism (AFLP) markers in 42 populations and seven pairs of congeneric plant species occurring sympatrically in the same geographic region
Summary
The genetic diversity of species and populations has multiple implications for their ecology, evolution and survival. An increasing number of recent studies are showing, that genetic diversity (i.e., depending on variation in DNA nucleotide sequence) is not the only heritable genomic information that could influence the ecology, evolution or survival of populations. There is a growing consensus that natural epigenetic diversity could endow wild plant populations with an extra layer of heritable phenotypic variation that could complement genetically-based variation and contribute to local adaptation and survival (Grativol et al 2012; Medrano et al 2014; Schulz et al 2014; Herrera et al 2017; Gáspár et al 2019; but see Herden et al 2019). More studies with non-model plants growing in a real-world context are essential to understand the potential role of epigenetic variation in plant adaptation and in ecological and evolutionary processes
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