Conservation Epigenetics – will it come or will it go?

The human-induced 6th mass extinction threatens more species with global extinction than ever before with an average of around 25 % of species in assessed animal and plant groups being threatened. That means, that up to one million species already face extinction, many of which in the next decades, unless action is taken to reduce the intensity of drivers of biodiversity loss (Díaz et al. 2019). Conservation biology has been the research field that deals with this biodiversity crisis. It studies the conservation of biodiversity by investigating the biology of species, communities, and ecosystems that are directly or indirectly threatened by human activities or other agents. Its goal is to provide principles and tools for preserving all levels of biodiversity including its evolutionary potential (Soulé 1985). Conservation genetics in turn, is a well-established scientific field within conservation biology and is dedicated to shedding light on the evolutionary dimension of conservation biology. Large numbers of scientific studies are published each year in dedicated scientific journals as well as journals targeting broader scientific audiences (Holderegger et al. 2019). Conservation genetics has impacted conservation on two levels. First, it established mechanistic principles that have acted as conservation guidelines already for decades – from the core principle that genetic diversity is crucial for the well-being of populations to central concepts such as inbreeding depression, accumulation and loss of deleterious mutations, loss of genetic variation in small populations, genetic adaptation to captivity and its effect on reintroduction success, outbreeding depression (Frankham 1996), minimum viable populations (Menges 1991), and the distinctness of rear edge populations in conservation (Hampe and Petit 2005). Besides such textbook principles, the availability of conservation genetic tools directly empowers conservation managers on the ground including barcoding and metabarcoding for species identification or monitoring or with genetic studies on gene flow to assess fragmentation and connectivity to assess the success of connectivity measures (Holderegger et al. 2019). Still, Holderegger and co-workers attest that conservation genetics still remains a largely academic field and that real‐world examples with a clear focus on application would largely be restricted to emblematic vertebrate fauna. They observe, that this gap between conservation genetic sciences and the practical conservation yet increases through the rapid development of high‐throughput genotyping technologies and thus the use of genomic information as new challenges emerge with regards to data analyses. Undeniably, despite these initial gaps between science and management, the genomic revolution will provide valuable information for conservation genetic approaches, as it will allow to focus on a species’ or population’s adaptive potential to respond to stress by means of molecular changes (Eizaguirre & Baltazar-Soares, 2014).

In a recent review, Rey et al. propose to establish yet another research field that will contribute to conservation biology, namely conservation epigenetics. They argue that epigenetic marks – more particularly DNA methylation – and developmental reprogramming should be considered as an additional conservation level stating that DNA methylation is sensitive to the environment and is involved in organisms' plastic and adaptive responses to changing environments. As we have seen in previous chapters, epigenetic elements can act in conjunction with genetic information to modulate phenotypes during development (Allis & Jenuwein, 2016). Moreover, while some epigenetic patterns are under genetic determinism, some others are directly modulated by the surrounding environmental conditions (Feil & Fraga, 2012), particularly that of DNA methylation. Thus, DNA methylation induced by environmental stressors during development that produces maladaptive phenotypes can have negative consequences in populations (Piferrer, 2016). Rey et al. argue, that accounting for such epigenetic trap effect faced by some populations could be useful in a conservation context. Specifically, at the population level, modifications of DNA methylation patterns among individuals in response to changing environment could be associated with a phenotypic shift from suboptimal to optimal value in the resulting environment, hence leading to adaptive phenotypic plasticity corresponding to the environmentally induced phenotype variation (EPV) (Rey et al. 2019 and references therein). Alternatively, environmental changes could potentially induce spontaneous and random modifications in DNA methylation patterns potentially resulting in the broadening of phenotypic values around the original mean phenotype within populations corresponding to the stochastic developmental phenotype variation (SPV) (Rey et al. .2019 and references therein). They further argue, that those two processes can lead to phenotypic diversification, with EPV being expected to be selected when environmental changes are predictable allowing organisms to quickly respond and adjust their phenotypes to maximize their fitness while SPV could be considered a random and non-directional flexibilization of genome expression to new and/or unpredictable environments constituting a bet-hedging strategy resulting in the maintenance of few individuals harboring optimal phenotypes and most individuals expressing suboptimal phenotypes in the new environment (Rey et al. 2019 and references therein).

However, as we have seen throughout this book, the ecological importance of variation in DNA methylation relative to genetic variation has only been established in a few individual case studies and still needs to be empirically quantified in non-model plant species (Richards et al. 2017). That said, the growing body of literature shows that the distribution and especially function of DNA methylation variation varies strongly among taxa and its role in acclimation is not as straight forward as seen for genetic variation in adaptation. Therefore, it will likely take at least another decade to establish sound evidence for a large variety of conservation relevant taxa for conservation epigenetics to become effective. And given that sound epigenetic research is necessarily based on omics resources, a conservation epigenetic toolbox will likely not be available for conservation practitioners in the near future. As with the beginnings of conservation genetics decades ago, our current understanding of plant epigenetics might still be sufficient to establish basic principles for conservation management.