The Genomic Processes of Biological Invasions: From Invasive Species to Cancer Metastases and Back Again

Abstract

The concept of invasion is useful across a broad range of contexts, spanning from the fine scale landscape of cancer tumors up to the broader landscape of ecosystems. Invasion biology provides extraordinary opportunities for studying the mechanistic basis of contemporary evolution at the molecular level. Although the field of invasion genetics was established in ecology and evolution more than 50 years ago, there is still a limited understanding of how genomic level processes translate into invasive phenotypes across different taxa in response to complex environmental conditions. This is largely because the study of most invasive species is limited by information about complex genome level processes. We lack good reference genomes for most species. Rigorous studies to examine genomic processes are generally too costly. On the contrary, cancer studies are fortified with extensive resources for studying genome level dynamics and the interactions among genetic and non-genetic mechanisms. Extensive analysis of primary tumors and metastatic samples have revealed the importance of several genomic mechanisms including higher mutation rates, specific types of mutations, aneuploidy or whole genome doubling and non-genetic effects. Metastatic sites can be directly compared to primary tumor cell counterparts. At the same time, clonal dynamics shape the genomics and evolution of metastatic cancers. Clonal diversity varies by cancer type, and the tumors’ donor and recipient tissues. Still, the cancer research community has been unable to identify any common events that provide a universal predictor of “metastatic potential” which parallels findings in evolutionary ecology. Instead, invasion in cancer studies depends strongly on context, including order of events and clonal composition. The detailed studies of the behavior of a variety of human cancers promises to inform our understanding of genome level dynamics in the diversity of invasive species and provide novel insights for management.

Genomic data is missing for many highly invasive species, restricting our preparedness for escalating incursion rates

“…This has resulted in broad understanding of the evolutionary processes associated with invasion, such as the general effects of bottlenecks and genetic drift on invasion success and the specific adaptive responses of some invasive species 27 . However, much invasive biology research still suffers from a lack of information around complex processes operating at the genomic level 28 , 29 . Moving from a ‘genetic’ (single or few loci) lens to a genome-wide (‘genomic’) one can improve analytical accuracy in some scenarios 30 .…”

Rapid phenotypic differentiation and local adaptation in Japanese knotweed s.l. (Reynoutria japonicaandR. ×bohemica, Polygonaceae) invading novel habitats

“…Epigenetic effects have been shown to be especially important in response to hybridization and exposure to stressful or novel environments, which are circumstances often experienced by invasive plants (Mounger et al, 2021). The chance sampling of genotypes involved in the invasion process, combined with non-genetic sources of phenotypic variation, can lead to divergence in phenotypes of these populations even in the absence of abundant genetic variation (Keller and Taylor, 2008; Prentis et al, 2008; Neinavaie et al, 2021). Considering the plurality of potential mechanisms of rapid evolution in novel conditions, studies that examine phenotypic response of clonal replicates in natural settings will enhance our understanding of the processes of adaptation.…”

Genetic and Epigenetic Differentiation Across Intertidal Gradients in the Foundation Plant Spartina alterniflora

“…The importance of genetically based variation within species has been well accepted in the field of evolutionary biology, but further analyses are required to understand the mechanisms that enable organisms to adapt to conditions in novel or challenging environments. In addition to patterns of genetic variation that have been associated with different environmental challenges (Bock et al, 2015;Hodgins et al, 2015;Neinavaie et al, 2021), increasing evidence suggests that epigenetic variation (e.g., alterations to DNA methylation, small RNAs, and chromatin remodeling) plays a role in ecology, and that this variation can be both environmentally induced and contribute to phenotypic plasticity (Cortijo et al, 2014;Medrano et al, 2014;Robertson and Richards, 2015;Banta and Richards, 2018;Ashe et al, 2021;Mounger et al, 2021a;Stajic and Jansen, 2021). This additional source of variation may be particularly important for sessile organisms such as plants, given that individuals are unable to migrate away from stressors (Dodd and Douhovnikoff, 2016;Balao et al, 2018).…”