Inter-annual and spatial climatic variability have led to a balance between local fluctuating selection and wide-range directional selection in a perennial grass species

Abstract

Background and aims: The persistence of a plant population under a specific local climatic regime requires phenotypic adaptation with underlying particular combinations of alleles at adaptive loci. The level of allele diversity at adaptive loci within a natural plant population conditions its potential to evolve, notably towards adaptation to a change in climate. Investigating the environmental factors that contribute to the maintenance of adaptive diversity in populations is thus worthwhile. Within-population allele diversity at adaptive loci can be partly driven by the mean climate at the population site but also by its temporal variability.

Methods: The effects of climate temporal mean and variability on within-population allele diversity at putatively adaptive quantitative trait loci (QTLs) were evaluated using 385 natural populations of Lolium perenne (perennial ryegrass) collected right across Europe. For seven adaptive traits related to reproductive phenology and vegetative potential growth seasonality, the average within-population allele diversity at major QTLs (HeA) was computed.

Key results: Significant relationships were found between HeA of these traits and the temporal mean and variability of the local climate. These relationships were consistent with functional ecology theory.

Conclusions: Results indicated that temporal variability of local climate has likely led to fluctuating directional selection, which has contributed to the maintenance of allele diversity at adaptive loci and thus potential for further adaptation.

Keywords: Lolium perenne; Allele diversity; adaptive diversity; climatic adaptation; fluctuating selection; genome-wide genotyping; grassland; intra-specific variability; natural genetic diversity; perennial ryegrass.

Fig. 1.

Spatial distribution across Europe of the within-population trait-associated diversity criterion of heading in first year (i.e. heading without vernalization requirements) (HeA_HFY) computed for 183 natural populations of perennial ryegrass. The pairing of dot colours and HeA_HFY ranges is given in the inset.

Fig. 2.

Within-population trait-associated diversity criterion (HeA) of each studied trait (ordinate) plotted against the most significant climate indicator (abscissa) in the best multiple regression model predicting this criterion. (A) Aftermath heading (AHD), (B) heading date (HDT), (C) heading in first year (HFY), (D) summer canopy height (SMH), (E) spring canopy height (SPH), (F) winter growth score (WGS) and (G) yearly cumulated canopy height (YCH). meanPCi and stdPCi are the ith principal components of the PCAs of norms of climatic variables and of inter-annual standard deviations of climatic variables, respectively. The Pearson correlation coefficient (r) between the HeA criterion and the climate indicator is displayed as well as the percentage of variance explained by the climate indicator (partial R² estimated by subtracting the coefficient of determination of the complete model without the targeted climate indicator from the one of complete model including the targeted climate indicator). The coefficient of determination of the complete model (with all retained climate indicators) is also displayed (model R²). The red diamonds represent the regression line or curve (polynomial of degree 2) of the within-population trait-associated diversity criterion (HeA) on the climate indicator when all other climate indicators in the multiple regression model are set to their mean values.