Phenotypes of Pinus sylvestris are more coordinated under local harsher conditions across Europe

Abstract

Plant species that grow across environmental gradients show a range of trait expression, but traits do not vary independently. In fact, phenotypes are integrated expressions of multiple traits that covary due to trade‐offs among functions and processes. Understanding trait covariation structures will ultimately help with predicting species' responses to change and developing management actions. We measured variation and covariation (a proxy of phenotypic integration) among functional traits of Pinus sylvestris from paired populations across its European distribution. Populations within a pair were close enough to be in gene flow contact but located in contrasting environmental conditions across a local gradient. Measured traits represented three axes of variation (groups of traits) related to a tree's competitive ability and the trade‐off between resource acquisition and conservation, namely plant size measures and stem and foliar traits. Results revealed important intra‐ and inter‐population trait variability. In particular, at the population level, trait means shifted across the climatic gradient mainly described by mean annual temperature. Moreover, we found a higher degree of trait covariation in populations under harsher environments (i.e. lower environmental suitability for the species). This pattern was consistent within population pairs, suggesting that higher trait covariation may be adaptive, being more coordinated in sites with harsher conditions. At larger spatial scales, we found a less conclusive pattern with a trend of increasing covariation at the northern edge of the species distribution. This result suggests that at larger scales different processes may be involved in the trade‐off between the adaptive value of phenotypic covariation versus its constraints on trait combinations that may limit plant's response capability. Synthesis. Trait covariation varies at different spatial scales, increasing under harsher conditions, and the robustness and repeatability of this pattern suggests its adaptive role for the species' responses to different environments.

Phenotypic integration does not constrain phenotypic plasticity: differential plasticity of traits is associated to their integration across environments

“…Several authors have suggested that stress should lead to higher phenotypic integration, if a tighter and more coordinated phenotype is favoured when resources are limiting (Schlichting, 1986; Gianoli, 2004; Gianoli & Palacio‐López, 2009). However, the adaptive value of increased integration in stress is yet to be determined (Pigliucci, 2003; Merilä & Björklund, 2004; but see Benavides et al ., 2021). Indeed, studies showing the adaptive value of phenotypic integration, regardless of stress level, are very scarce (Damián et al ., 2020).…”

Depicting the phenotypic space of the annual plant Diplotaxis acris in hyperarid deserts

“…Furthermore, we also know how fast annual plant populations can change their genetic composition in just a few years due to selection and/or demography (Gómez et al, 2018 ; Kuester et al, 2016 ; Nevo et al, 2012 ; Van Dijk & Hautekèete, 2014 ; Vigouroux et al, 2011 ). On top of that, harsher environments might promote higher phenotypic plasticity (Exposito‐Alonso et al, 2018 ; Lázaro‐Nogal et al, 2015 ; Matesanz et al, 2020 ) and tighter phenotypic integration (Benavides et al, 2021 ; Dwyer & Laughlin, 2017 ; Michelaki et al, 2019 ). For all these reasons, we believe that most annuals will have a chance to thrive in a warmer, more arid, and more seasonal environments by shifting their phenotypic spaces toward new scenarios in which phenotypic integration and seed‐related traits will acquire a higher relevance.…”

“…Over generations, a population molds its genetic composition and builds its phenotypic space (Fraebel et al, 2017 ; Murren, 2012 ; Pigliucci, 2007 ; Schlichting & Pigliucci, 1995 ), which encompasses the assemblage of trait combinations of well‐suited phenotypes. One way to understand how the phenotypic space is structured deals with the quantification of among‐ and within‐population genetic variations in phenotypic traits as well as the intrapopulation correlation pattern among traits (Benavides et al, 2021 ; Messier et al, 2018 ). At the population scale, correlations among traits mainly reflect genetic, developmental, or physiological processes (Armbruster et al, 2014 ; Messier et al, 2018 ).…”

“…Regardless of the several ways in which natural selection determines the distribution of phenotypes within a population, along with the omnipresent random effects of genetic drift, the severity of the environment eventually imposes the ecological limits of the phenotypic space. Field studies in plants revealed how environmental gradients (e.g., elevation and core–periphery clines) influenced mean trait values and also the pattern of trait covariation within populations (Benavides et al, 2021 ; Boucher et al, 2013 ; Dwyer & Laughlin, 2017 ; Michelaki et al, 2019 ; Rosas et al, 2019 ; Umaña & Swenson, 2019 ). Furthermore, some of these studies did show how the degree of phenotypic integration, given by the strength of covariation among traits, intensified with increasing environmental harshness (Dwyer & Laughlin, 2017 ; Michelaki et al, 2019 ; Benavides et al, 2021 ; but see Boucher et al, 2013 ).…”

“…Field studies in plants revealed how environmental gradients (e.g., elevation and core–periphery clines) influenced mean trait values and also the pattern of trait covariation within populations (Benavides et al, 2021 ; Boucher et al, 2013 ; Dwyer & Laughlin, 2017 ; Michelaki et al, 2019 ; Rosas et al, 2019 ; Umaña & Swenson, 2019 ). Furthermore, some of these studies did show how the degree of phenotypic integration, given by the strength of covariation among traits, intensified with increasing environmental harshness (Dwyer & Laughlin, 2017 ; Michelaki et al, 2019 ; Benavides et al, 2021 ; but see Boucher et al, 2013 ). Although these field studies were not exclusively focused on life history traits and did not quantify the underlying genetic component of phenotypic integration, they shed light on the consequences of intraspecific trait variability and phenotypic integration in natural populations for plant community assembly and ecosystem functioning.…”