Abstract

The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and nongenetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the nongenetic 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 anthropogenic environmental changes. Several studies have documented landscape-level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of nongenetic variation. To assess one type of nongenetic 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; 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. In addition, 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.

Highlights

  • Preserving the ability of populations to respond to environmental challenges is critical to conservation efforts

  • We used a multivariate test for homogeneity of dispersions to estimate epigenetic diversity, that is, variation in DNA methylation levels, for the maternal trees and offspring datasets following the approach of Anderson et al (2006), which measures the average distance from each individual to their group centroid in a multivariate space using a dissimilarity measure. In line with this interpretation, we argue that the distance from each individual sample to its population centroid in a multivariate space generated using an epigenetic distance matrix provides an estimate of the extent of the variation in DNA methylation, that is, epigenetic variation

  • To test how much of the epigenetic differentiation could be attributed to differences among populations, and how much of the epigenetic variation was associated with the populations after controlling for differences in sequence variation physically linked to the epigenetic variation, we modeled the average DNA methylation level of each 50–250 bp long fragment in response to the sequence context (CTXT), the population (POP) and its interaction with context (CTXT:POP), and the genotype of the fragment (GENO) and its interaction with context (CTXT:GENO) fitted in this order

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Summary

Introduction

Preserving the ability of populations to respond to environmental challenges is critical to conservation efforts. This ability depends on phenotypic variation (Björklund et al, 2009; Henn et al, 2018; Norberg et al, 2001). Sultan (2015) argued that as modern biologists our task is to restore the context dependence of gene expression and trait variation. This task has become relevant in the context of anthropogenic alterations to natural ecosystems. In the framework of re‐evaluating the mapping of genotype to phenotype (Keller, 2014; Pigliucci, 2010), we can use the concepts of Evo‐Devo to explore phenotypic plasticity and genetic and nongenetic structure within populations, as well as examine how these processes are impacted by climate change (Campbell et al, 2017)

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