Biological invasion: The influence of the hidden side of the (epi)genome

Abstract

Understanding the mechanisms underlying biological invasions and rapid adaptation to global change remains a fundamental challenge, particularly in small populations lacking in genetic variation. Two understudied mechanisms that could facilitate adaptive evolution and adaptive plasticity are the increased genetic variation due to transposable elements (TEs), and associated or independent modification of gene expression through epigenetic changes. Here, we focus on the potential role of these genetic and non‐genetic mechanisms for facilitating invasion success. Because novel or stressful environments are known to induce both epigenetic changes and TE activity, these mechanisms may play an underappreciated role in generating phenotypic and genetic variation for selection to act on. We review how these mechanisms operate, the evidence for how they respond to novel or stressful environments, and how these mechanisms can contribute to the success of biological invasions by facilitating adaptive evolution and phenotypic plasticity. Because genetic and phenotypic variations due to TEs and epigenetic changes are often well regulated or “hidden” in the native environment, the independent and combined contribution of these mechanisms may only become important when populations colonize novel environments. A focus on the mechanisms that generate and control the expression of this variation in new environments may provide insights into biological invasions that would otherwise not be obvious. Global changes and human activities impact on ecosystems and allow new opportunities for biological invasions. Invasive species succeed by adapting rapidly to new environments. The degree to which rapid responses to environmental change could be mediated by the epigenome—the regulatory system that integrates how environmental and genomic variation jointly shape phenotypic variation—requires greater attention if we want to understand the mechanisms by which populations successfully colonize and adapt to new environments. A free Plain Language Summary can be found within the Supporting Information of this article.

A Potential Role for Phenotypic Plasticity in Invasions and Declines of Social Insects

“…Epigenetic mechanisms have also been suggested to be relevant in facilitating phenotypic changes associated with invasion; for example in house sparrows increased variation in genome-wide DNA methylation was detected in invasive populations in Kenya (Liebl et al, 2013), and in invasive ascidians and corals, methylation changes quickly occurred in response to environmental challenges (Putnam et al, 2016;Huang et al, 2017). Epigenetic mechanisms are particularly relevant for the success of biological invasions as they can produce new variation (and therefore adaptation) even in the lack of genetic diversity (Hawes et al, 2018), and even more so when combined with plasticity in other regulators of genetic activity, such as non-coding RNAs or transposable elements (Stapley et al, 2015;Marin et al, 2019). Epigenetic mechanisms have also been a topic of substantial interest in social insects, where they have been demonstrated to be relevant to caste plasticity, worker division of labor, and learning and memory in social insects (Glastad et al, 2019).…”

Hypomethylation of the aquatic invasive plant, Ludwigia grandiflora subsp. hexapetala mimics the adaptive transition into the terrestrial morphotype

“…This definition broadly encompasses several levels of chromatin modifications, including DNA methylation, histone modifications and variants, and non-coding RNAs (Duncan et al 2014, Allis andJenuwein 2016). It has recently been suggested that epigenetics is a potential source of flexibility involved in the success of invasive species, allowing organisms to express advantageous phenotypes across a broader range of environments (Richards 2006, Richards et al 2017, for a recent review see Marin et al 2019).…”

Drosophila suzukiioxidative stress response involvesJhehgene cluster but not transposable elements

“…The rapid spread of invasive species in a huge spectrum of environments relies on multiple factors, from genetics to phenotypic plasticity, probably including fine molecular mechanism such as hormonal production or epigenetic gene regulation (Beldade et al , 2011; Marin et al , 2019; Stapley et al , 2015). Phenotypic plasticity, i.e., the ability of a genotype to express different phenotypes in different environments (Ghalambor et al , 2015) has been proposed as one of the most promising explanations for invasive success, particularly in the case of founder population depleted of genetic variation (Estoup et al , 2016; Marin et al , 2019). Among deleterious environments that can be encountered by invasive species, oxidative stress caused by phytosanitary products is one of them.…”