Drivers of population differentiation in phenotypic plasticity in a temperate conifer: A 27‐year study

Abstract

Phenotypic plasticity is a main mechanism for organisms to cope with changing environments and broaden their ecological range. Plasticity is genetically based and can evolve under natural selection, such that populations within a species show distinct phenotypic responses to the environment if evolved under different conditions. Understanding how intraspecific variation in phenotypic plasticity arises is critical to assess potential adaptation to ongoing climate change. Theory predicts that plasticity is favored in more favorable but variable environments. Yet, many theoretical predictions about benefits, costs, and selection on plasticity remain untested. To test these predictions, we took advantage of three genetic trials in the northern Rocky Mountains, USA, which assessed 23 closely located Pinus ponderosa populations over 27 years. Mean environmental conditions and their spatial patterns of variation at the seed source populations were characterized based on six basic climate parameters. Despite the small area of origin, there was significant genetic variation in phenotypic plasticity for tree growth among populations. We found a significant negative correlation between phenotypic plasticity and the patch size of environmental heterogeneity at the seed source populations, but not with total environmental spatial variance. These results show that populations exposed to high microhabitat heterogeneity have evolved higher phenotypic plasticity and that the trigger was the grain rather than the total magnitude of spatial heterogeneity. Contrary to theoretical predictions, we also found a positive relationship between population plasticity and summer drought at the seed source, indicating that drought can act as a trigger of plasticity. Finally, we found a negative correlation between the quantitative genetic variance within populations and their phenotypic plasticity, suggesting compensatory adaptive mechanisms for the lack of genetic diversity. These results improve our understanding of the microevolutionary drivers of phenotypic plasticity, a critical process for resilience of long‐lived species under climate change, and support decision‐making in tree genetic improvement programs and seed transfer strategies.

Variation and plasticity in life-history traits and fitness of wild Arabidopsis thaliana populations are not related to their genotypic and ecological diversity

“…Our second expectation dealt with the effects of genotypic and ecological diversity on phenotypic plasticity of A. thaliana traits, which was supported by the positive relationship between environmental heterogeneity and phenotypic plasticity found in other plants [31,32,85,86]. Our common garden experiments, carried out under unplanned benign and harsh conditions for A. thaliana, allowed us to estimate the response of maternal lines from each population to warmer temperatures and more seasonal precipitation (Fig.…”

“…Thus, we also hypothesized that differences in the ecological diversity of populations promoted lower and higher phenotypic variation in populations with low and high genotypic diversity, respectively. On top of the effects of fine-scale selection on fitness-related traits in heterogeneous environments [25][26][27][28][29], which promote within-population phenotypic variation, phenotypic plasticity has also been seen to be enhanced in environments with higher levels of ecological heterogeneity [30][31][32]. In addition, environmental maternal effects may also provide transgenerational adaptive plasticity in plants [33][34][35][36].…”

Plasticity in growth is genetically variable and highly conserved across spatial scales in a Mediterranean pine

“…Phenotypic plasticity can be advantageous under some conditions and disadvantageous or not advantageous under others (Alpert & Simms, 2002). Thus, populations living in contrasting environments may express diverging plasticity patterns, triggering extensive genetic variation in plasticity within plant species (Matesanz et al ., 2019; de la Mata et al ., 2022). Accounting for this among‐population differentiation in plasticity may be crucial to accurately forecast the impact of global change on plant species (Patsiou et al ., 2020).…”

Identifying genetic variation associated with environmental gradients and drought‐tolerance phenotypes in ponderosa pine

“…Adaptation to local climate conditions has been considered typical for tree populations (Kitzmiller, 2005 ; Langlet, 1971 ; Wright, 2007 ; Ying & Liang, 1994 ), but organisms with such long generation times and a sessile lifestyle can become maladapted if environmental shifts rapidly occur (Aitken et al., 2008 ; Alberto et al., 2013 ; Benomar et al., 2022 ; Frank et al., 2017 ; Gougherty et al., 2021 ). Plants also exhibit plastic changes in their growth form and physiology in response to stress, and the level of plasticity can itself be heritable (Auld et al., 2010 ; de la Mata et al., 2022 ; Van Kleunen & Fischer, 2005 ; Wu et al., 2023 ; Zeng et al., 2017 ) and may be under the selection (Zettlemoyer & Peterson, 2021 ). Understanding the distribution of genetic variation related to environmental responses may help us better predict changes and manage forests in a shifting climate (Leites & Benito Garzón, 2023 ; Neale & Kremer, 2011 ; Oney et al., 2013 ; Razgour et al., 2019 ).…”