Correlated evolution between climate and suites of traits along a fast–slow continuum in the radiation ofProtea

Abstract

Evolutionary radiations are responsible for much of Earth's diversity, yet the causes of these radiations are often elusive. Determining the relative roles of adaptation and geographic isolation in diversification is vital to understanding the causes of any radiation, and whether a radiation may be labeled as “adaptive” or not. Across many groups of plants, trait–climate relationships suggest that traits are an important indicator of how plants adapt to different climates. In particular, analyses of plant functional traits in global databases suggest that there is an “economics spectrum” along which combinations of functional traits covary along a fast–slow continuum. We examine evolutionary associations among traits and between trait and climate variables on a strongly supported phylogeny in the iconic plant genus Protea to identify correlated evolution of functional traits and the climatic‐niches that species occupy. Results indicate that trait diversification in Protea has climate associations along two axes of variation: correlated evolution of plant size with temperature and leaf investment with rainfall. Evidence suggests that traits and climatic‐niches evolve in similar ways, although some of these associations are inconsistent with global patterns on a broader phylogenetic scale. When combined with previous experimental work suggesting that trait–climate associations are adaptive in Protea, the results presented here suggest that trait diversification in this radiation is adaptive.

Microscale trait‐environment associations in two closely‐related South African shrubs

“…Since the site is in a fire‐dominated biome, the plants are also roughly the same age, adding another layer of standardization. Previous analyses using a single leaf per plant have detected significant trait‐environment associations in this group (Carlson et al., , ; Carlson and Holsinger, ; Prunier et al., ; Mitchell et al., , ). We measured traits commonly used in the literature and used in previous genus‐wide evolutionary analyses in Protea , i.e., leaf fresh water content (FWC), plant height (HEIGHT), leaf area (LA), leaf length‐to‐width ratio (LWR), leaf mass per area (LMA), and stomatal density (SD) (Table , Appendix S2).…”

“…Previous work in Protea has found evidence for genus‐wide, clade level, and intraspecific trait‐environment associations with physiological and fitness consequences suggesting local adaptation (Carlson et al., ; Prunier et al., ; Heschel et al., ; Mitchell et al., , ). The traits linked to environmental gradients also have fitness consequences within wild populations (Carlson et al., ).…”

“…Although global generalizations across taxa are valuable, they also leave large amounts of variation in trait values unexplained, and they may not reflect the evolutionary processes that are responsible for that variation (Cavender‐Bares et al., ; Mason and Donovan, ). Trait‐environment patterns also may differ across regions with similar biomes (Forrestel et al., ), within regions (Cavender‐Bares et al., ; Mitchell et al., ), among species within communities (Lajoie and Vellend, ), among species within genera (Cavender‐Bares et al., ; Mason and Donovan, ; Mitchell et al., ), or across populations of a single species (Carlson et al., ; Baruch et al., ).…”

Climate explains population divergence in drought-induced plasticity of functional traits and gene expression in a South AfricanProtea

“…Although heat stress can be detrimental, in the CFR cold stress may impose a stronger selective pressure for growth (Wilson et al 2015). In fact, in a study of 56 Proteaceae species looking at climate and plant trait correlations, Mitchell et al, showed the most strongly supported evolutionary correlations to be between winter minimum temperature (next to mean annual temperature and elevation) and plant height (Mitchell et al 2018). They also note that this negative effect of elevation on plant height might be coupled potentially with shallower soils in the high elevation sites (Campbell & Werger 1988).…”

“…Our study species, Protea repens (common sugar bush), is part of a lineage that has radiated over the past 5 to 18 million years to produce 112 species, ~85% of which are endemic (Rebelo 2001; Sauquet et al 2009). Along the environmental gradients Protea species inhabit, we have evidence for local adaptation and context-dependent benefits in several traits (Latimer et al 2009; Carlson et al 2011, 2016; Prunier et al 2012; Akman et al 2016; Mitchell et al 2018). There is also evidence for differential developmental plasticity and drought plasticity in leaf traits of several other Protea species ( Protea sect.…”