A multi-dimensional selective landscape drives adaptive divergence between and within closely related Phlox species

Selection causes local adaptation across populations within species and simultaneously divergence between species. However, it is unclear if either the force of or the response to selection is similar across these scales. We show that natural selection drives divergence between closely related species in a pattern that is distinct from local adaptation within species. We use reciprocal transplant experiments across three species of Phlox wildflowers to characterize widespread adaptive divergence. Using provenance trials, we also find strong local adaptation between populations within a species. Comparing divergence and selection between these two scales of diversity we discover that one suite of traits predicts fitness differences between species and that an independent suite of traits predicts fitness variation within species. Selection drives divergence between species, contributing to speciation, while simultaneously favoring extensive diversity that is maintained across populations within a species. Our work demonstrates how the selection landscape is complex and multidimensional.

Methods
These data are phenotypic measurements of three species of Phlox plants grown in three common gardens. We included 122 genotypes of Phlox amoena amoena (eight populations), 125 genotypes of Phlox pilosa pilosa (nine populations), and 37 genotypes of Phlox pilosa deamii (three populations) from throughout their native ranges for our common garden experiment. Each plant was propigated and clonaly replicated to include at least one clone in each of three field sites. Each field site included four blocks with randomized plants withint each block. We monitored fitness-related traits in the gardens over the course of three growing seasons between planting in April 2018 and final data collection in September 2020.We recorded damage from large vertebrate herbivores as a binary trait (0 = herbivore damage, 1 = no herbivore damage). We counted the total number of open flowers on each plant on a weekly basis from beginning of April through beginning of June 2019. Flowers on these taxa remain open and fresh for about one week, so our timing minimized double counting or missing flowers. We counted the total number of fruits set by each plant including both mature fruits that remained on the plant as well as open calyces where fruits had already shattered. In October 2019, we harvested all aboveground biomass for each plant, leaving root systems and the stem at the base of each plant intact consistent with the annual aboveground die-back that these taxa experience each winter. We dried this tissue in a drying oven at 60° C for 48 hours before measuring the mass with an electronic scale. Due to the Covid-19 pandemic, we were not able to return to the gardens again until September 2020 when we recorded final survival.