Genome size reduction can trigger rapid phenotypic evolution in invasive plants.

Abstract

The study of rapid evolution in invasive species has highlighted the fundamental role played by founder events, emergence of genetic novelties through recombination and rapid response to new selective pressures. However, whether rapid adaptation of introduced species can be driven by punctual changes in genome organization has received little attention. In plants, variation in genome size, i.e. variation in the amount of DNA per monoploid set of chromosomes through loss or gain of repeated DNA sequences, is known to influence a number of physiological, phenological and life-history features. The present study investigated whether change in genome size has contributed to the evolution of greater potential of vegetative growth in invasive populations of an introduced grass. The study was based on the recent demonstration that invasive genotypes of reed canarygrass (Phalaris arundinacea) occurring in North America have emerged from recombination between introduced European strains. The genome sizes of more than 200 invasive and native genotypes were measured and their genome size was related to their phenotypic traits measured in a common glasshouse environment. Population genetics data were used to infer phylogeographical relationships between study populations, and the evolutionary history of genome size within the study species was inferred. Invasive genotypes had a smaller genome than European native genotypes from which they are derived. This smaller genome size had phenotypic effects that increased the species' invasive potential, including a higher early growth rate, due to a negative relationship between genome size and rate of stem elongation. Based on inferred phylogeographical relationships of invasive and native populations, evolutionary models were consistent with a scenario of genome reduction by natural selection during the invasion process, rather than a scenario of stochastic change. Punctual reduction in genome size could cause rapid changes in key phenotypic traits that enhance invasive ability. Although the generality of genome size variation leading to phenotypic evolution and the specific genomic mechanisms involved are not known, change in genome size may constitute an important but previously under-appreciated mechanism of rapid evolutionary change that may promote evolutionary novelties over short time scales.