Inheritance of DNA methylation differences in the mangrove Rhizophora mangle

Abstract

The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and non-genetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the non-genetic contributions to variation. Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions, and is potentially threatened by climate change. Several studies have documented landscape level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of non-genetic variation. To assess one type of non-genetic variation, we examined the patterns of DNA sequence and DNA methylation in maternal plants and offspring from natural populations of R. mangle from the Gulf Coast of Florida. We used a reduced representation bisulfite sequencing approach (epi-genotyping by sequencing or epiGBS) to address the following questions: a) What are the levels of genetic and epigenetic diversity in natural populations of R. mangle? b) How are genetic and epigenetic variation structured within and among populations? c) How faithfully is epigenetic variation inherited? We found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field and that a large portion (up to ~25%) of epigenetic differences among offspring grown in common garden was explained by maternal family. Therefore, epigenetic variation could be an important source of response to challenging environments in the genetically depauperate populations of this foundation species.

Conservation biology meets evo‐devo: How understanding the emergence of variation can inform its management

“…This will likely cause us to increasingly aim towards understanding the contribution of nongenetic variation to phenotypic variation in natural populations, which will be highly relevant within a changing world. Indeed, this is well demonstrated by Mounger et al (2021), whose study incorporates the important view that the ability of populations to persist is determined by their continued ability to produce phenotypic variation (regardless of mechanism). However, they suggest we move beyond the view that only DNA‐based variation is important for adaptation and as a conservation target.…”

Response to nitrogen and salinity in Rhizophora mangle propagules varies by maternal family and population of origin

“…We previously reported low genetic diversity among these plants based on molecular markers, which is expected to limit the potential for different responses among individuals. On the other hand, we discovered high epigenetic diversity (Mounger et al, 2021), which could contribute to phenotypic and functional diversity, and could be a mechanism underlying the type of phenotypic differences and plasticity we found here (Zhang et al, 2013;Nicotra et al, 2015;Herrera et al, 2017;Jueterbock et al, 2020). In addition, we know very little about the interactions with the microbiome in the species, but microbes have been highlighted as important symbionts in these and other challenging environments (Bowen et al, 2017;Angermeyer et al, 2018;Jung et al, 2021).…”

“…We sampled six populations of R. Honeymoon Island had a near monoculture of R. mangle while the remaining sites contained mixtures of two other mangrove species that are common in Florida: Laguncularia racemosa L. and Avicennia germinans L.. We refer to plants from different sites as members of different populations based on our previous work which found differences among sites based on molecular markers (Mounger et al, 2021). At each population, we collected 20 propagules directly from each of 10 maternal trees separated by at least 10 m from each other to maximize the range of genetic variation sampled within each population (Albrecht et al, 2013).…”

“…Further, some epigenetic differences have been shown to be heritable. In fact, we discovered that the differences in DNA methylation in R. mangle propagules were predicted by maternal tree suggesting a high degree of heritability of differences in DNA methylation (Mounger et al, 2021).…”

“…On the other hand, we found that nearby populations had low genetic diversity, and little population differentiation. Instead we discovered high epigenetic diversity based on DNA methylation polymorphisms (Mounger et al, 2021). This type of epigenetic diversity has been associated with phenotypic and functional diversity, and could be a mechanism underlying phenotypic plasticity (Zhang et al, 2013; Nicotra et al, 2015; Herrera et al, 2017; Jueterbock et al, 2020).…”