Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species

Abstract

Rapid adaptation of invasive species to novel habitats has puzzled evolutionary biologists for decades, especially as this often occurs in the face of limited genetic variability. Although some ecological traits common to invasive species have been identified, little is known about the possible genomic/genetic mechanisms that may underlie their success. A common scenario in many introductions is that small founder population sizes will often lead to reduced genetic diversity, but that invading populations experience large environmental perturbations, such as changes in habitat and environmental stress. Although sudden and intense stress is usually considered in a negative context, these perturbations may actually facilitate rapid adaptation by affecting genome structure, organization and function via interactions with transposable elements (TEs), especially in populations with low genetic diversity. Stress-induced changes in TE activity can alter gene action and can promote structural variation that may facilitate the rapid adaptation observed in new environments. We focus here on the adaptive potential of TEs in relation to invasive species and highlight their role as powerful mutational forces that can rapidly create genetic diversity. We hypothesize that activity of transposable elements can explain rapid adaptation despite low genetic variation (the genetic paradox of invasive species), and provide a framework under which this hypothesis can be tested using recently developed and emerging genomic technologies.

Genetic variability of Colobanthus quitensis from King George Island (Antarctica)

“…On the genetic level, one of the main mechanisms associated with response to stress factors is the activation of the transposable elements (TE) (McClintock 1984;Capy et al 2000;Schrader et al 2014;Makarevitch et al 2015). Increasing numbers of TE copies in response to the stress factors has been thought to be associated with decreased fitness through increased lethality (Wilke et al 1992;Charlesworth et al 1994;Stapley et al 2015). However, it was proved for many plant species that the tendency of TE to insert into repetitive DNA mitigates their deleterious potential (SanMiguel et al 1996;Kalendar et al 1999;Suoniemi et al 1997;Ramsay et al 1999).…”

The ghost of introduction past: Spatial and temporal variability in the genetic diversity of invasive smallmouth bass

“…Invasive species are particularly suitable for demographic analyses, as they frequently experience rapid alternations in levels of genetic diversity following introduction (Chown et al., 2015; Hui & Richardson, 2017; Lee, 2002; Rius & Darling, 2014; Roman & Darling, 2007). To this end, the assessment of genetic diversity has become essential for establishing the demographic and adaptive potential of populations in novel environments (Dlugosch, Anderson, Braasch, Cang, & Gillette, 2015; Prentis, Wilson, Dormontt, Richardson, & Lowe, 2008; Stapley, Santure, & Dennis, 2015; Zenni, Bailey, & Simberloff, 2014) and provides insight into the role that genetic variability plays in an organisms’ invasive success (Edelaar et al., 2015). Ultimately, this information allows predictions to be made on population viability, aiding in the development of an appropriate, species‐specific management strategy (Chown et al., 2015; Meyer et al., 2017; Prentis et al., 2008).…”

Variación génica intrapoblacional del caracol gigante africano (Achatina fulica) en el Valle del Cauca

“…El caracol africano como especie invasora, presenta a nivel genético el mismo comportamiento que las demás especies invasoras (13)(14)(15): una baja en la diversidad génica respecto a las poblaciones en su rango natural de distribución en África, debido al efecto fundador que ocurre en cada evento de introducción, y a los cuellos de botella subsiguientes al establecimiento y aclimatación a las condiciones del nuevo hábitat (1,4). Aunque desde el punto de vista ecológico las poblaciones de A. fulica en las etapas iniciales de invasión pueden considerarse exitosas, cuando la invasión lleva varias décadas la dinámica poblacional tiende a estabilizarse o incluso puede llegar a decaer de forma natural (1,15).…”

“…Aunque desde el punto de vista ecológico las poblaciones de A. fulica en las etapas iniciales de invasión pueden considerarse exitosas, cuando la invasión lleva varias décadas la dinámica poblacional tiende a estabilizarse o incluso puede llegar a decaer de forma natural (1,15). Para explicar este fenómeno se han formulado varias hipótesis, desde causas genómicas, de amplia plasticidad fenotípica, comportamentales o múltiples introducciones que compensan la deriva génica en la que entran los individuos fundadores (14,15).…”

“…Likemost other invasive species (13)(14)(15), the giant African snail shows low genetic diversity compared with the populations in its natural distribution range in Africa, due to a founder effect that occurs at each introduction event, and to the bottlenecks that occur after establishment and acclimation to the conditions of the new habitat (1,4). Although from the ecological point of view A. fulica populations can be considered successful at their initial invasion stages, the population dynamics tend to stabilize or even decay naturally several decades after the invasion (1,15).…”