Adaptation to invasions: when does it occur?

Despite the negative impacts on biodiversity, ecosystems and human wellbeing, biological invasions also offer a unique opportunity to investigate population evolution in a timescale compatible with human life. Indeed, many mechanisms are known to be involved in the ability of non-indigenous species (NIS) to survive, establish and spread in the habitats. These mechanisms are particularly interesting when the invading population establishes and becomes invasive starting from a small propagule, a process that gave rise to the concept of “genetic paradox”. Founder events and genetic bottlenecks related to the introduction of NIS would be expected to decrease the genetic variability of the introduced population, thus reducing the invaders’ ability to persist and spread in the novel environment. Many mechanisms are known to play a role in the ability of the introduced organisms to adapt to the new habitat. Still, there is a general lack of focus on the chronological order in which these mechanisms operate. In this review, we define three temporal stages in which adaptation to invasion can take place, and for each stage, we show which mechanisms of adaptation are involved and how they operate. The first stage is in the native range, where many forms of preadaptation to the invasion may evolve: pre-adaptation may be due, for example, to the evolution of phenotypic plasticity, or it can be mediated by human activities (the so-called “Anthropogenically Induced Adaptation to Invade”), or it may even be related to life-history traits of the (future) invader. Our second stage corresponds to the founding event, during which genetic bottlenecks can alter the genetic pool of invading organisms, with (not consistently negative) consequences on their fitness. The second stage also includes the captivity/ cultivation phases, during which genetic admixture between genetically-differentiated individuals is possible and could help the invaders overcome the loss of genetic variability associated with the founding event; however, the admixture process is mainly investigated after the introduction (third phase). Lastly, once in the new habitat, introduced organisms can undergo adaptation thanks to various processes: among these, we find the activity of transposable elements (TEs) and epigenetic modifications (such asDNAmethylation); furthermore, NIS’ adaptation can be facilitated by the human alteration of natural environments. Of the three temporal phases we identified, the first and third phases are the most studied and relevant during invasions. To date, there is no mammalian study regarding the second phase. Despite the numerous mechanisms known to be involved in the adaptation of NIS to the new habitat, and despite the abundance of studies which aim to shed light on the “genetic paradox”, works on mammal species are scanty, and most of the mechanisms of adaptation remain uninvestigated in this animal group. In particular, a large part of current literature investigating the process of adaptation in non-indigenous mammals regards their behavioral plasticity and capacity to solve the new problems faced in the introduction range. This is not surprising, given the cognitive abilities of mammal species; however, other mechanisms such as epigenetic modifications and TEs activation following introduction still remain unexplored in mammal invaders, and there seems to be no reason why they should not be relevant in the context of biological invasions.