How woody plants adjust above- and below-ground traits in response to sustained drought.

Future increases in drought severity and frequency are predicted to have substantial impacts on plant function and survival. However, there is considerable uncertainty concerning what drought adjustment is and whether plants can adjust to sustained drought. This review focuses on woody plants and synthesises the evidence for drought adjustment in a selection of key above-ground and below-ground plant traits. We assess whether evaluating the drought adjustment of single traits, or selections of traits that operate on the same plant functional axis (e.g. photosynthetic traits) is sufficient, or whether a multi-trait approach, integrating across multiple axes, is required. We conclude that studies on drought adjustments in woody plants might overestimate the capacity for adjustment to drier environments if spatial studies along gradients are used, without complementary experimental approaches. We provide evidence that drought adjustment is common in above-ground and below-ground traits; however, whether this is adaptive and sufficient to respond to future droughts remains uncertain for most species. To address this uncertainty, we must move towards studying trait integration within and across multiple axes of plant function (e.g. above-ground and below-ground) to gain a holistic view of drought adjustments at the whole-plant scale and how these influence plant survival.

Genomic data and common garden experiments reveal climate-driven selection on ecophysiological traits in two Mediterranean oaks.

Improving our knowledge of how past climate-driven selection has acted on present-day trait population divergence is essential to understand local adaptation processes and improve our predictions of evolutionary trajectories in the face of altered selection pressures resulting from climate change. In this study, we investigated signals of selection on traits related to drought tolerance and growth rates in two Mediterranean oak species (Quercus faginea and Q. lusitanica) with contrasting distribution ranges and climatic niches. We genotyped 182 individuals from 24 natural populations of the two species using restriction-site-associated DNA sequencing and conducted a thorough functional characterization in 1602 seedlings from 21 populations cultivated in common garden experiments under contrasting watering treatments. Our genomic data revealed that both Q. faginea and Q. lusitanica have very weak population genetic structure, probably as a result of high rates of pollen-mediated gene flow among populations and large effective population sizes. In contrast, common garden experiments showed evidence of climate-driven divergent selection among populations on traits related to leaf morphology, physiology and growth in both species. Overall, our study suggests that climate is an important selective factor for Mediterranean oaks and that ecophysiological traits have evolved in drought-prone environments even in a context of very high rates of gene flow among populations.

Multi-trait genetic variation in resource-use strategies and phenotypic plasticity correlates with local climate across the range of a Mediterranean oak (Quercus faginea).

Resource-use strategies are hypothesized to evolve along climatic gradients. However, our understanding of the environmental factors driving divergent evolution of resource-use strategies and the relationship between trait genetic variation and phenotypic plasticity is far from complete. Using the Mediterranean tree Quercus faginea as study system, we tested the hypothesis that a conservative resource-use strategy with increased drought tolerance and reduced phenotypic plasticity has evolved in areas with longer and more severe dry seasons. We conducted a glasshouse experiment in which we measured leaf morphological, physiological, growth and allocation traits in seedlings from 10 range-wide climatically contrasting populations, grown under two different watering treatments. Both univariate and multivariate analyses revealed a genetic gradient of resource-use strategies and phenotypic plasticity associated with provenance climate. In particular, populations from harsher (drier and colder) environments had more sclerophyllous leaves, lower growth rates, better physiological performance under dry conditions and reduced multi-trait phenotypic plasticity compared to populations from more mesic and milder environments. Our results suggest that contrasting precipitation and temperature regimes play an important role in the adaptive intraspecific evolution of multivariate phenotypes and their plasticity, resulting in coordinated morphology, physiology, growth and allometry according to alternative resource-use strategies.

Adaptive responses to temperature and precipitation variation at the early-life stages of Pinus sylvestris.

Early-stage fitness variation has been seldom evaluated at broad scales in forest tree species, despite the long tradition of studying climate-driven intraspecific genetic variation. In this study, we evaluated the role of climate in driving patterns of population differentiation at early-life stages in Pinus sylvestris and explored the fitness and growth consequences of seed transfer within the species range. We monitored seedling emergence, survival and growth over a 2-yr period in a multi-site common garden experiment which included 18 European populations and spanned 25° in latitude and 1700 m in elevation. Climate-fitness functions showed that populations exhibited higher seedling survival and growth at temperatures similar to their home environment, which is consistent with local adaptation. Northern populations experienced lower survival and growth at warmer sites, contrary to previous studies on later life stages. Seed mass was higher in populations from warmer areas and was positively associated with survival and growth at more southern sites. Finally, we did not detect a survival-growth trade-off; on the contrary, bigger seedlings exhibited higher survival probabilities under most climatic conditions. In conclusion, our results reveal that contrasting temperature regimes have played an important role in driving the divergent evolution of P. sylvestris populations at early-life stages.

Selection patterns on early-life phenotypic traits in Pinus sylvestris are associated with precipitation and temperature along a climatic gradient in Europe.

Understanding the dynamics of selection is key to predicting the response of tree species to new environmental conditions in the current context of climate change. However, selection patterns acting on early recruitment stages and their climatic drivers remain largely unknown in most tree species, despite being a critical period of their life cycle. We measured phenotypic selection on Pinus sylvestris seed mass, emergence time and early growth rate over 2 yr in four common garden experiments established along the latitudinal gradient of the species in Europe. Significant phenotypic plasticity and among-population genetic variation were found for all measured phenotypic traits. Heat and drought negatively affected fitness in the southern sites, but heavy rainfalls also decreased early survival in middle latitudes. Climate-driven directional selection was found for higher seed mass and earlier emergence time, while the form of selection on seedling growth rates differed among sites and populations. Evidence of adaptive and maladaptive phenotypic plasticity was found for emergence time and early growth rate, respectively. Seed mass, emergence time and early growth rate have an adaptive role in the early stages of P. sylvestris and climate strongly influences the patterns of selection on these fitness-related traits.

Correlated evolution of morphology, gas exchange, growth rates and hydraulics as a response to precipitation and temperature regimes in oaks (Quercus).

It is hypothesised that tree distributions in Europe are largely limited by their ability to cope with the summer drought imposed by the Mediterranean climate in the southern areas and by their competitive potential in central regions with more mesic conditions. We investigated the extent to which leaf and plant morphology, gas exchange, leaf and stem hydraulics and growth rates have evolved in a coordinated way in oaks (Quercus) as a result of adaptation to contrasting environmental conditions in this region. We implemented an experiment in which seedlings of 12 European/North African oaks were grown under two watering treatments, a well-watered treatment and a drought treatment in which plants were subjected to three cycles of drought. Consistent with our hypothesis, species from drier summers had traits conferring more tolerance to drought such as small sclerophyllous leaves and lower percent loss of hydraulic conductivity. However, these species did not have lower growth rates as expected by a trade-off with drought tolerance. Overall, our results revealed that climate is an important driver of functional strategies in oaks and that traits have evolved along two coordinated functional axes to adapt to different precipitation and temperature regimes.

Increased root investment can explain the higher survival of seedlings of 'mesic' Quercus suber than 'xeric' Quercus ilex in sandy soils during a summer drought.

In Mediterranean-type ecosystems, drought is considered the main ecological filter for seedling establishment. The evergreen oaks Quercus ilex L. and Quercus suber L. are two of the most abundant tree species in the Mediterranean Basin. Despite their shared evergreen leaf habit and ability to resist low soil water potentials, traditionally it has been suggested that Q. ilex is better suited to resist dry conditions than Q. suber. In this study, we examined how seedlings of Q. ilex and Q. suber grown in sandy soils responded to different levels of water availability using natural dry conditions and supplemental watering. Specifically, we estimated survival and water status of seedlings and explored the role of acorn mass and belowground biomass in seedling performance. To our surprise, Q. suber was better able to survive the summer drought in our experiment than Q. ilex. Nearly 55% of the Q. suber seedlings remained alive after a 2-month period without rain or supplemental water, which represents almost 20% higher survival than Q. ilex over the same period. At the end of the dry period, the surviving seedlings of Q. suber had strikingly higher water potential, potential maximum quantum yield of photosystem II (Fv/Fm) and stomatal conductance (gs) than those of Q. ilex. Acorn mass was associated with the probability of survival under dry conditions; however, it did not explain the differences in survival or water status between the species. In contrast, Q. suber had a higher root ratio and root:shoot ratio than Q. ilex and these traits were positively associated with predawn leaf water potential, Fv/Fm, gs and survival. Taken together, our results suggest that the higher relative investment in roots by Q. suber when growing in a sandy acidic substrate allowed this species to maintain better physiological status and overall condition than Q. ilex, increasing its probability of survival in dry conditions.

Adaptive consequences of human-mediated introgression for indigenous tree species: the case of a relict Pinus pinaster population.

Human-induced gene movement via afforestation and restoration programs is a widespread phenomenon throughout the world. However, its effects on the genetic composition of native populations have received relatively little attention, particularly in forest trees. Here, we examine to what extent gene flow from allochthonous plantations of Pinus pinaster Aiton impacts offspring performance in a neighboring relict natural population and discuss the potential consequences for the long-term genetic composition of the latter. Specifically, we conducted a greenhouse experiment involving two contrasting watering treatments to test for differences in a set of functional traits and mortality rates between P. pinaster progenies from three different parental origins: (i) local native parents, (ii) exotic parents and (iii) intercrosses between local mothers and exotic fathers (intraspecific hybrids). Our results showed differences among crosses in cumulative mortality over time: seedlings of exotic parents exhibited the lowest mortality rates and seedlings of local origin the highest, while intraspecific hybrids exhibited an intermediate response. Linear regressions showed that seedlings with higher water-use efficiency (WUE, δ(13)C) were more likely to survive under drought stress, consistent with previous findings suggesting that WUE has an important role under dry conditions in this species. However, differences in mortality among crosses were only partially explained by WUE. Other non-measured traits and factors such as inbreeding depression in the relict population are more likely to explain the lower performance of native progenies. Overall, our results indicated that intraspecific hybrids and exotic individuals are more likely to survive under stressful conditions than local native individuals, at least during the first year of development. Since summer drought is the most important demographic and selective filter affecting tree establishment in Mediterranean ecosystems, a potential early selective advantage of exotic and hybrid genotypes would enhance initial steps of introgression of non-native genes into the study relict population of P. pinaster.

Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities.

Plants distributed across a wide range of environmental conditions are submitted to differential selective pressures. Long-term selection can lead to the development of adaptations to the local environment, generating ecotypic differentiation. Additionally, plant species can cope with this environmental variability by phenotypic plasticity. In this study, we examine the importance of both processes in coping with environmental heterogeneity in the Mediterranean sclerophyllous cork oak Quercus suber. For this purpose, we measured growth and key functional traits at the leaf level in 9-year-old plants across 2 years of contrasting precipitation (2005 and 2006) in a common garden. Plants were grown from acorns originated from 13 populations spanning a wide range of climates along the distribution range of the species. The traits measured were: leaf size (LS), specific leaf area (SLA), carbon isotope discrimination (Delta(13)C) and leaf nitrogen content per unit mass (N(mass)). Inter-population differences in LS, SLA and Delta(13)C were found. These differences were associated with rainfall and temperature at the sites of origin, suggesting local adaptation in response to diverging climates. Additionally, SLA and LS exhibited positive responses to the increase in annual rainfall. Year effect explained 28% of the total phenotypic variance in LS and 2.7% in SLA. There was a significant genotype x environment interaction for shoot growth and a phenotypic correlation between the difference in shoot growth among years and the annual mean temperature at origin. This suggests that populations originating from warm sites can benefit more from wet conditions than populations from cool sites. Finally, we investigated the relationships between functional traits and aboveground growth by several regression models. Our results showed that plants with lower SLA presented larger aboveground growth in a dry year and plants with larger leaf sizes displayed larger growth rates in both years. Overall, the study supports the adaptive value of SLA and LS for cork oak under a Mediterranean climate and their potentially important role for dealing with varying temperature and rainfall regimes through both local adaptation and phenotypic plasticity.