Weak phylogenetic and climatic signals in plant heat tolerance

Abstract

AimHigh heat tolerance is a potential way for plants to maintain performance under high temperatures that can be acted upon by environmental filters to influence community assembly. Plant heat tolerances are phenotypically plastic and thus common garden experiments are needed to test if species from hotter environments have consistently higher heat tolerance than species from colder environments. Past studies that have measured heat tolerance from species grown in common gardens have found conflicting relationships between species' climatic origins and their heat tolerance, possibly due to phylogenetic non‐independence of study species. In this study, we test the hypothesis that phylogenetic structure can help to explain variation in heat tolerance in order to resolve the confliciting relationships between climate and plant heat tolerance.LocationFairchild Tropical Botanic Garden and the Gifford Arboretum, Miami, FL, USA.TaxonPteridophytes, Gymnosperms and Angiosperms.MethodsWe tested for phylogenetic signal in the photosynthetic heat tolerance of 123 species of ferns, gymnosperms, magnoliids, monocots and eudicots by calculating Blomberg's K. Phylogenetic independent contrasts of heat tolerance and climatic distributions for >100 species were used to test the hypothesis that climate can predict variation in heat tolerance.ResultsSpecies' heat tolerances were not phylogenetically conserved according to Blomberg's K, but we found significant differences in the heat tolerance of ferns, gymnosperms, magnoliids, monocots and eudicots. When controlling for phylogenetic non‐independence, we found a significant, but weak relationship between the mean maximum temperature of the warmest month of species' climatic distributions and their photosynthetic heat tolerance.Main conclusionsWe conclude that phylogeny and climate are weak predictors of photosynthetic heat tolerance. However, differences among the groups we studied suggest that the variation in heat tolerance may be better explained by differences in microenvironment, thermoregulatory traits and leaf temperatures.

Leaf heat tolerance of 147 tropical forest species varies with elevation and leaf functional traits, but not with phylogeny

“…Species‐level replication was limited in the current study, and if intraspecific variation would be significant, greater replication could potentially slightly change heat tolerance estimates and therefore affect the phylogenetic analysis. Nonetheless, the absence of strong phylogenetic patterns in heat tolerance is in accordance with other recent studies (Lancaster & Humphreys, 2020; Perez & Feeley, 2021). Furthermore, the predominance of plasticity over evolutionary legacies is consistent with the plasticity in the temperature relations of other aspects of metabolism in trees from the aseasonal lowland tropics, such as the convergence of the optimum temperature for photosynthesis on local mean temperatures in diverse forest communities (Slot & Winter, 2017a), and acclimation of photosynthesis (Slot & Winter, 2017b) and leaf respiration (Cheesman & Winter, 2013; Slot et al, 2014) to experimental warming.…”

“…Our approach was based on the protocol that Krause et al (2010) developed to study leaf heat tolerance of (Panamanian) tropical trees. The protocol yields results that are very similar to those obtained in classical necrosis tests (Krause et al, 2010), and is now commonly used (e.g., Feeley, Martinez‐Villa, et al, 2020; Leon‐Garcia & Lasso, 2019; Perez & Feeley, 2020, 2021; Slot et al, 2019; Tiwari et al, 2021). We measured F v / F m on leaf disks 24 hr after they were incubated for 15 min in a temperature‐controlled water bath, using 8–12 incubation temperatures between 44°C and 54°C (where necessary 58°C), with a minimum of five leaf disks at each temperature.…”

“…Later studies reported more variation in heat tolerance, with both lower and higher values being observed in the early 20th century (Sapper, 1935), but it remained challenging to identify general patterns underlying this variation. In recent years, leaf heat tolerance has received renewed interest as ongoing global warming and more frequent and intense heatwaves may push ecosystems past their critical thermal thresholds (Feeley et al, 2020; Geange et al, 2021; Lancaster & Humphreys, 2020; Perez & Feeley, 2020, 2021). Recent studies have shown that heat tolerance increases from the poles toward the tropics (O'Sullivan et al, 2017) and from high elevation to low elevation (Feeley, Martinez‐Villa, et al, 2020), in parallel with increasing temperatures under which plants develop.…”

Photosystem II heat tolerances characterize thermal generalists and the upper limit of carbon assimilation

“…The heat tolerance of plants' photosystem II (PSII) photochemistry may provide a useful estimate of the upper thermal limit of photosynthesis and has the potential to explain the physiological mechanisms underlying some of the ecological responses of plants to climate change (Clark, Piper, Keeling, & Clark, 2003; Doughty & Goulden, 2009; Feeley, Bravo‐Avila, Fadrique, Perez, & Zuleta, 2020; Mau, Reed, Wood, & Cavaleri, 2018; Pau, Detto, Kim, & Still, 2018). Higher heat tolerance of PSII photochemistry is generally assumed to allow for improved growth, reproduction and/or survival in hot environments, presumably by facilitating photosynthesis at high temperatures (Feeley, Martinez‐villa, Perez & Duque 2020; Krause, Winter, Krause, & Virgo, 2015; Tiwari et al, 2020; but see Perez & Feeley, 2020a, 2020b). However, these assumptions have not been widely tested, and it is unclear how PSII heat tolerance integrates with different thermal strategies for understanding the effects of climate change on plants.…”

“…Higher heat tolerance of PSII photochemistry is generally assumed to allow for improved growth, reproduction and/or survival in hot environments, presumably by facilitating photosynthesis at high temperatures (Feeley, Martinez-villa, Perez & Duque 2020;Krause, Winter, Krause, & Virgo, 2015;Tiwari et al, 2020; but see Perez & Feeley, 2020a, 2020b. However, these assumptions have not been widely tested, and it is unclear how PSII heat tolerance integrates with different thermal strategies for understanding the effects of climate change on plants.…”