Recent and ancient evolutionary events shaped plant elemental composition of edaphic endemics: a phylogeny‐wide analysis of Iberian gypsum plants

Abstract

Summary The analysis of plant elemental composition and the underlying factors affecting its variation are a current hot topic in ecology. Ecological adaptation to atypical soils may shift plant elemental composition. However, no previous studies have evaluated its relevance against other factors such as phylogeny, climate or individual soil conditions. We evaluated the effect of the phylogeny, environment (climate, soil), and affinity to gypsum soils on the elemental composition of 83 taxa typical of Iberian gypsum ecosystems. We used a new statistical procedure (multiple phylogenetic variance decomposition, MPVD) to decompose total explained variance by different factors across all nodes in the phylogenetic tree of target species (covering 120 million years of Angiosperm evolution). Our results highlight the relevance of phylogeny on the elemental composition of plants both at early (with the development of key preadaptive traits) and recent divergence times (diversification of the Iberian gypsum flora concurrent with Iberian gypsum deposit accumulation). Despite the predominant phylogenetic effect, plant adaptation to gypsum soils had a strong impact on the elemental composition of plants, particularly on sulphur concentrations, while climate and soil effects were smaller. Accordingly, we detected a convergent evolution of gypsum specialists from different lineages on increased sulphur and magnesium foliar concentrations.

Gypsum endemics accumulate excess nutrients in leaves as a potential constitutive strategy to grow in grazed extreme soils

“…Plant affinity for gypsum soils is related to a particular elemental composition. Similar to previous studies, gypsum endemics had higher leaf S and sometimes higher Ca and Mg concentrations than generalist species (Merlo et al, 2019;Muller et al, 2017;Palacio et al 2007Palacio et al , 2022. This singular elemental composition is a constitutive nutritional strategy of gypsum endemics regardless of whether they grow in calcareous or gypsum soils .…”

Global patterns and drivers of leaf photosynthetic capacity: The relative importance of environmental factors and evolutionary history

“…This new paradigm could be applied to other plant traits. For example, studies focusing on multi-elemental concentrations and secondary metabolites have also consistently demonstrated the dominant role of evolutionary history in explaining the large-scale variability in various leaf traits (Asner et al, 2014;Palacio et al, 2022;Sardans et al, 2015Sardans et al, , 2021Vallicrosa, Sardans, Maspons, & Peñuelas, 2022;Vallicrosa, Sardans, Maspons, Zuccarini, et al, 2022). Given that both evolutionary history information and current environmental factors jointly regulate large-scale variability in plant functional traits, including V c,max25 , our results further suggest that the variability stored in the species and phylogeny must be credited, in addition to the site-associated current environmental factors, to estimate and project the global V c,max25 variability accurately.…”

“…We address these questions by testing the following hypotheses: (1) V c,max25 could vary across different vegetated biomes and life‐forms, with higher values in grasslands relative to shrublands and forests and in fast‐growing relative to slow‐growing species, because the former plant types usually have higher nutrient concentrations that are often related to more investment in photosynthetic apparatus (Ali et al, 2016; Kattge et al, 2009; Smith & Dukes, 2018); (2) V c,max25 could show a significant phylogenetic signal, given that V c,max25 has been connected previously with multiple biotic factors (i.e., RuBisCO kinetic parameters and photosynthesis‐associated leaf nutrient concentrations) that all display strong phylogenetic regulation (Galmes et al, 2015; Huang et al, 2022; Jump & Peñuelas, 2005; Liu et al, 2022; Sardans et al, 2021); and (3) the global patterns of V c,max25 could be regulated jointly by both current environmental factors and long‐term evolutionary history, with the latter being the dominant driver, because mounting evidence suggests a more important contribution of species identity information to the variability of photosynthesis‐associated leaf nutrient concentrations than environmental factors (Asner et al, 2014; Dahlin et al, 2013; Palacio et al, 2022; Sardans et al, 2021; Vallicrosa, Sardans, Maspons, & Peñuelas, 2022; Vallicrosa, Sardans, Maspons, Zuccarini, et al, 2022). To test these three hypotheses, we first collated a global dataset of field‐measured V c,max25 for C 3 plants with concurrent measurements of present‐day environmental factors (i.e., climate and soil variables), then integrated this unique global dataset with multiple statistical modelling analyses detailed below.…”

Nutritional strategy underlying plant specialization to gypsum soils

“…Gypsophiles generally display a unique foliar composition with a remarkable accumulation of excess nutrients from gypsum soils in above-ground organs ( Palacio et al 2022 ). Accordingly, gypsophiles display higher foliar S and Mg (and marginally higher Ca) and lower K concentrations than gypsovags ( Palacio et al 2007 , 2022 ).…”

“…However, gypsophiles differ from gypsovags by their foliar composition, accumulating elements found in excess in gypsum soils, as do other edaphic specialists with their sister generalist taxa. This foliar composition is shared by gypsophiles from different families and regions of the world ( Duvigneaud and Denaeyer-De Smet 1966 ; Alvarado 1995 ; Palacio et al 2007 , 2022 ; Bolukbasi et al 2016 ; Muller et al 2017 ; Merlo et al 2019 ). In contrast to the well-known physiological tolerance mechanism of other soil specialists, the physiological and ecological role of the foliar composition of gypsophiles remains elusive ( Cera et al 2021 b ).…”