Increased genetic variation and evolutionary potential drive the success of an invasive grass

Abstract

Despite the increasing biological and economic impacts of invasive species, little is known about the evolutionary mechanisms that favor geographic range expansion and evolution of invasiveness in introduced species. Here, we focus on the invasive wetland grass Phalaris arundinacea L. and document the evolutionary consequences that resulted from multiple and uncontrolled introductions into North America of genetic material native to different European regions. Continental-scale genetic variation occurring in reed canarygrass' European range has been reshuffled and recombined within North American introduced populations, giving rise to a number of novel genotypes. This process alleviated genetic bottlenecks throughout reed canarygrass' introduced range, including in peripheral populations, where depletion of genetic diversity is expected and is observed in the native range. Moreover, reed canarygrass had higher genetic diversity and heritable phenotypic variation in its invasive range relative to its native range. The resulting high evolutionary potential of invasive populations allowed for rapid selection of genotypes with higher vegetative colonization ability and phenotypic plasticity. Our results show that repeated introductions of a single species may inadvertently create harmful invaders with high adaptive potential. Such invasive species may be able to evolve in response to changing climate, allowing them to have increasing impact on native communities and ecosystems in the future. More generally, multiple immigration events may thus trigger future adaptation and geographic spread of a species population by preventing genetic bottlenecks and generating genetic novelties through recombination.

Fig. 1.

Regional-level (Left, a–d) and population-level (Right, e–h) statistics of genetic diversity for invasive regions (black/hatched black histograms) and native regions (gray/hatched gray histograms) of reed canarygrass. Regional-level statistics are: overall percentage of polymorphic loci (a), overall allelic richness (b), weighted overall gene diversity (c), and genetic differentiation between populations (d) for both neutral markers (Fst_[pop]) and phenotypic traits (Qst_[pop]). Population-level statistics are: mean percentage of polymorphic loci (e), mean allelic richness (f), corrected Shannon–Wiener index for genotypic diversity (g), and mean richness in multilocus genotypes (h). Error bars represent standard errors. Letters indicate means that were not significantly different at the 5% level after a 10,000-permutation test.

Fig. 2.

Geographic distribution of neutral genetic diversity of reed canarygrass for five highly variable allozyme loci (among 12 studied). Pie charts display allele frequencies within central vs. southern regions of occurrence in the native range (Czech Republic vs. France) and invasive range (Vermont vs. North Carolina) of reed canarygrass. Note that alleles unique to southern France (DIA-2d and IDH-1b) and the Czech Republic (PGI-2d, UGPP-1c, and PGM-1b) cooccur within invasive regions of reed canarygrass.

Fig. 3.

The number of multilocus genotypes (G) of reed canarygrass detected in central and peripheral regions of its invasive range (Vermont and North Carolina, respectively) and native range (Czech Republic and France, respectively), as a function of sample size. Dot–dash lines represent 95% confidence limits obtained by randomly generating 50,000 replicates of G for every sample size. This permutation procedure was used to assess the robustness of regional patterns of genotypic diversity to unevenness in sample size.

Fig. 4.

Dynamics of emergence (a), vegetative spread (b), leaf production (c), and final biomass production (d) of 90 genotypes sampled in the four study regions: Vermont, North Carolina, the Czech Republic, and France. Means and standard errors (error bars) were back-transformed fitted values from generalized linear models (see Materials and Methods and SI Table 2 for model structure). Best models explaining the data were determined by AIC-based model selection (see SI Table 2).

Fig. 5.

Broad-sense heritability (a) and phenotypic plasticity (b) of phenotypic traits within populations of reed canarygrass sampled from its invasive and native range. (a) Broad-sense heritability was computed from a greenhouse experiment using clones of 90 genetically distinct genotypes, as the ratio H² = V_G/(V_G+V_E), where V_G is the within-population genetic variance and V_E is the environmental variance. Error bars represent 95% confidence intervals obtained by bootstrapping 1,000 draws of genotypes. (b) Phenotypic plasticity was computed from a field experiment, where clones of 36 genotypes were transplanted along a moisture gradient, as the ratio PV = (V_GxE + V_E)/(V_GxE + V_E + V_G), where V_GxE is the variance associated with genotype by environment interactions, V_E is the environmental variance, and V_G is the genotypic variance. Error bars represent 95% confidence intervals obtained by jackknifing over genotypes. Morphological principal component (Morpho Princ Comp) is the score on the first axis of a PCA performed on all morphological traits.