Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana

Abstract

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216‐year time series of Arabidopsis thaliana accessions from across its native range and applied spatially varying coefficient models to quantify region‐specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space or through time. For example, δ15N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer‐ versus spring‐collected plants, consistent with a life history–physiology axis from slow‐growing winter annuals to fast‐growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.

Climate biogeography ofArabidopsis thaliana:linking distribution models and individual variation

“…For our analysis of climate anomaly effects on individual performance of herbarium specimens, we used the Climate Research Unit (CRU) TS 4.01 dataset, providing a global time series of monthly temperature and precipitation for the period 1900-2010 at a 0.5° resolution (Harris et al, 2014). From the CRU data we calculated the same bioclimatic parameters that we used in the Maxent distribution model, but in the CRU data these bioclimatic variables were specific to each individual herbarium specimen in the time period it was collected (Supplemental Methods) (DeLeo et al, 2020). We then calculated local anomalies for each of these variables by taking the observed value, subtracting mean across the entire time series, and dividing by the standard deviation (DeLeo et al, 2020).…”

“…From the CRU data we calculated the same bioclimatic parameters that we used in the Maxent distribution model, but in the CRU data these bioclimatic variables were specific to each individual herbarium specimen in the time period it was collected (Supplemental Methods) (DeLeo et al, 2020). We then calculated local anomalies for each of these variables by taking the observed value, subtracting mean across the entire time series, and dividing by the standard deviation (DeLeo et al, 2020).…”

“…We also used occurrence data (with coordinates and without flagged problems N=115,226) from the Global Biodiversity Information Facility (GBIF) to test model predictions in regions outside of the native range of Arabidopsis (downloaded 30 Dec 2020, Gbif.Org, 2020). We deem these occurrences as lower quality given that many have not had the species identity and location closely checked (DeLeo et al, 2020).…”

Competition × drought interactions change phenotypic plasticity and the direction of selection on Arabidopsis traits

“…Some published data suggest the potential for competition × climate interaction effects on performance (Baron et al , 2015; Campitelli et al , 2016), though the physiological basis of these interactions is largely unknown. Third, previous research has yielded insight into genetic and physiological mechanisms of drought adaptation, providing a basis for specific hypotheses about how moisture and competitive gradients interact to select for different traits (McKay et al , 2003; Juenger et al , 2010; Des Marais et al , 2012; Lovell et al , 2013; Kenney et al , 2014; Lasky et al , 2014, 2018; El‐Soda et al , 2015; Bac‐Molenaar et al , 2016; Dittberner et al , 2018; Exposito‐Alonso et al , 2018, 2019; DeLeo et al , 2020).…”

Competition-by-drought interactions change phenotypic plasticity and the direction of selection on Arabidopsis traits

“…Some published data suggest the potential for competition-by-climate interaction effects on 70 performance (Baron et al, 2015;Campitelli et al, 2016) though the physiological basis of these interactions is largely unknown. Third, previous research has yielded insight into genetic and physiological mechanisms of drought adaptation, providing a basis for specific hypotheses about how moisture and competitive gradients interact to select for different traits (McKay et al, 2003;Juenger et al, 2010;Des Marais et al, 2012;Lovell et al, 2013;Kenney et al, 2014;Lasky et 75 al., 2014Lasky et 75 al., , 2018El-Soda et al, 2015;Bac-Molenaar et al, 2016;Dittberner et al, 2018;Exposito-Alonso et al, 2018DeLeo et al, 2019).…”