How do threatened plant species with low genetic diversity respond to environmental stress? Insights from comparative conservation epigenomics and phenotypic plasticity

Abstract

Many threatened plants have low genetic diversity, which may reduce their capacity for genetically based adaptation, increasing their extinction risk. Non‐genetic variation (e.g. epigenomic modifications such as DNA methylation) and plasticity may facilitate the persistence of threatened plants, yet are rarely incorporated into conservation assessments. We present a case study investigating variation and plasticity in DNA methylation and phenotypic traits in four genetically depauperate species ofLeavenworthia (Brassicaceae), including one widespread species and one asexual, threatened species. We grew individuals from several maternal lines and populations per species in contrasting watering treatments, measured phenotypic traits and analysed DNA methylation using whole‐genome bisulphite sequencing. We addressed four questions: (1) How do patterns of DNA methylation differ within and among species? (2) Within species, how do phenotypic traits and patterns of DNA methylation vary in response to drought? (3) Does variation in DNA methylation correspond to phenotypic variation? (4) What are the implications for conservation? We found that taxa were epigenomically distinct and that each species exhibited variation in DNA methylation among populations that could be relevant for conservation. Within species, the DNA methylation response to environmental stress corresponded to its phenotypic response. Species differed in their DNA methylation and phenotypic responses to environmental stress, with the extent of plasticity possibly related to species geographic range size. We also found phenotypic and DNA methylation variation in the asexual, threatened species that may be relevant for conservation. Our results suggest that variation in DNA methylation may promote the persistence of genetically depauperate threatened plants, highlighting its potential as a novel conservation target to reduce extinction risk.

Decoupled genetic and epigenetic variation in the montane endemicErodium cazorlanum(Geraniaceae) and a widespread congener

“…In this study, we found absence of correlation between genetic and epigenetic distances across individuals in the two study species, supporting it would be worth to experimentally exploring their relative contribution to individual phenotypes and their plasticities under controlled environmental conditions (see e.g. Williams et al, 2023).…”

“…Understanding the sources of natural phenotypic variation is a crucial question in ecology and evolution. The idea that epigenetic diversity can compensate for reduced genetic diversity, promoting phenotypic variation through trait plasticity in response to environmental changes is relatively new (Balao et al, 2018; Bossdorf et al 2008; Richards et al, 2017; Richards, 2006; Williams et al, 2023). Trait plasticity can be particularly advantageous for sessile organisms such as plants, with limited escape strategies to face environmental perturbations and, thus, the magnitude and population structure of genetic and epigenetic diversities in plant species with disparate genomic and ecological features warrants comprehensive investigation (Anderson & Gezon, 2015; Herrera et al,2022; Richards et al, 2017; Szukala et al, 2023).…”

“…Such knowledge can help to optimize decisions in conservation (i.e. accurately evaluating the adaptive potential of populations, Lamka et al, 2022; Williams et al, 2023), or even predict how plant species would fare when introduced in foreign ecosystems (i.e., assess invasive potential, Hawes et al, 2018).…”