Rapid adaptive evolution in novel environments acts as an architect of population range expansion

Abstract

Colonization and expansion into novel landscapes determine the distribution and abundance of species in our rapidly changing ecosystems worldwide. Colonization events are crucibles for rapid evolution, but it is not known whether evolutionary changes arise mainly after successful colonization has occurred, or if evolution plays an immediate role, governing the growth and expansion speed of colonizing populations. There is evidence that spatial evolutionary processes can speed range expansion within a few generations because dispersal tendencies may evolve upwards at range edges. Additionally, rapid adaptation to a novel environment can increase population growth rates, which also promotes spread. However, the role of adaptive evolution and the relative contributions of spatial evolution and adaptation to expansion are unclear. Using a model system, red flour beetles (), we either allowed or constrained evolution of populations colonizing a novel environment and measured population growth and spread. At the end of the experiment we assessed the fitness and dispersal tendency of individuals originating either from the core or edge of evolving populations or from nonevolving populations in a common garden. Within six generations, evolving populations grew three times larger and spread 46% faster than populations in which evolution was constrained. Increased size and expansion speed were strongly driven by adaptation, whereas spatial evolutionary processes acting on edge subpopulations contributed less. This experimental evidence demonstrates that rapid evolution drives both population growth and expansion speed and is thus crucial to consider for managing biological invasions and successfully introducing or reintroducing species for management and conservation.

Eco‐evolution on the edge during climate change

“…Prober et al (2015) discuss a number of possible ways to select source populations for assisted migration. Assisted migration could slow range expansions by disrupting spatial sorting and local adaptation, as demonstrated in three lab experiments (conducted under idealized conditions) that reshuffled individuals within a range (Ochocki and Miller 2017, Szűcs et al 2017, Weiss-Lehman et al 2017. Assisted migration could slow range expansions by disrupting spatial sorting and local adaptation, as demonstrated in three lab experiments (conducted under idealized conditions) that reshuffled individuals within a range (Ochocki and Miller 2017, Szűcs et al 2017, Weiss-Lehman et al 2017.…”

“…Natural selection can favor individuals with higher fecundity or dispersal ability on the expanding range front because range-front populations are often released from intra-and inter-specific tradeoffs that constrain this evolution in the range center (Burton et al 2010, Gilman et al 2010, Phillips et al 2010a, Svenning et al 2014. Lab experiments also demonstrate dispersal evolution during range expansion and suggest evolution of dispersal and population growth rate can occur in three to four generations under idealized lab conditions (Fronhofer and Altermatt 2015, Williams et al 2016, Ochocki and Miller 2017, Szűcs et al 2017, Weiss-Lehman et al 2017, Van Petegem et al 2018. Lab experiments also demonstrate dispersal evolution during range expansion and suggest evolution of dispersal and population growth rate can occur in three to four generations under idealized lab conditions (Fronhofer and Altermatt 2015, Williams et al 2016, Ochocki and Miller 2017, Szűcs et al 2017, Weiss-Lehman et al 2017, Van Petegem et al 2018.…”

Potential limits to the benefits of admixture during biological invasion

“…For example, several studies have found evidence consistent with inbreeding depression in natural invading populations and its rescue by admixture (Bailey & McCauley, ; Keller et al, ; Mullarkey, Byers, & Anderson, ; Nolte, Gompert, & Buerkle, ; Rius & Darling, ; van Kleunen et al, ). It may be that founding populations with particularly low genetic variation and high genetic load, which would be predicted to benefit most from admixture, are relatively rare across species introductions as a whole, although admixture could provide substantial benefits to founding populations when severe genetic bottlenecks do occur, and these benefits may be realized over evolutionary time, which is not readily observed in experimental crosses (Szűcs et al, ; Szűcs, Melbourne, et al, ; Szűcs, Vahsen, et al, ; Wagner et al, ).…”

Influence of density and salinity on larval development of salt‐adapted and salt‐naïve frog populations

“…As population abundances increase and reduce the efficacy of adaptive traits, populations may undergo declines but recover once the expression of adaptive traits is no longer dampened by density‐dependent regulation. Presently, we are unaware of studies that investigate how density dependence and adaptation may interact to affect population dynamics under climate change scenarios, but similar dynamics may occur at the edges of species range expansions (Szűcs et al, ).…”