Intermediate degrees of synergistic pleiotropy drive adaptive evolution in ecological time

Abstract

Rapid phenotypic evolution of quantitative traits can occur within years, but its underlying genetic architecture remains uncharacterized. Here we test the theoretical prediction that genes with intermediate pleiotropy drive adaptive evolution in nature. Through a resurrection experiment, we grew Arabidopsis thaliana accessions collected across an 8-year period in six micro-habitats representative of that local population. We then used genome-wide association mapping to identify the single-nucleotide polymorphisms (SNPs) associated with evolved and unevolved traits in each micro-habitat. Finally, we performed a selection scan by testing for temporal differentiation in these SNPs. Phenotypic evolution was consistent across micro-habitats, but its associated genetic bases were largely distinct. Adaptive evolutionary change was most strongly driven by a small number of quantitative trait loci (QTLs) with intermediate degrees of pleiotropy; this pleiotropy was synergistic with the per-trait effect size of the SNPs, increasing with the degree of pleiotropy. In addition, weak selection was detected for frequent micro-habitat-specific QTLs that shape single traits. In this population, A. thaliana probably responded to local warming and increased competition, in part mediated by central regulators of flowering time. This genetic architecture, which includes both synergistic pleiotropic QTLs and distinct QTLs within particular micro-habitats, enables rapid phenotypic evolution while still maintaining genetic variation in wild populations.

The genetics underlying natural variation of plant–plant interactions, a beloved but forgotten member of the family of biotic interactions

“…thaliana (Brachi et al ., , ); and (iii) by demonstrating the in situ adaptive evolution of a highly genetically polymorphic local population of A . thaliana to increased interspecific competition in less than eight generations (Frachon et al ., ). Therefore, A .…”

“…We therefore argue that identifying genes that underlie natural variation of plant–plant interactions under natural conditions will be crucial for understanding the adaptation to the presence of neighbors, especially in wild species. Accordingly, a recent study reported for the first time (to our knowledge) a GWA mapping approach combined with an in situ phenotyping experiment of heterospecific interactions (Frachon et al ., ). In this study, 195 whole‐genome sequenced natural accessions collected in a highly genetically polymorphic local population of A .…”

“…thaliana in its natural communities) crossed with three contrasting soil types. Interestingly, a minor fraction of the SNPs the most highly associated with the response to the presence of P. annua was shared among the three soil types, stressing the need to consider the impact of abiotic conditions on the identification of the genetic bases underlying competitive ability in a heterospecific neighborhood (Frachon et al ., ). Further experiments conducted under natural conditions will undoubtedly help to unravel the complexity of the molecular and genetic bases underlying natural plant–plant interactions.…”

“…Finally, in agreement with other types of biotic interactions (Bartoli and Roux, ), the majority of QTL mapping studies ( n = 39) revealed a complex genetic architecture associated with plant–plant interactions (Figure ). The quantitative genetic architecture is highly diverse among plant–plant interacting systems, ranging from the identification of few medium‐effect QTLs to the identification of up to tens of small‐effect QTLs (Frachon et al ., ). A monogenic architecture was reported for the remaining eight QTL mapping studies, all focusing on the natural variation of response to parasitic plants in three crop species, i.e.…”

“…Therefore, in order to accelerate the identification of QTLs underlying natural variation of plant–plant interactions, we advocate the development of local mapping populations that are known to interact with other plant species and are genetically diverse. While such populations can be identified within wild species (Frachon et al ., ), this may remain an important challenge in major crops.…”