Local adaptation to aridity in a widely distributed angiosperm tree species is mediated by seasonal increase of sugars and reduced growth

Abstract

Abstract Trees in dry climates often have higher concentrations of total non-structural carbohydrates (NSC = starch + soluble sugars [SS]) and grow less than conspecifics in more humid climates. This pattern might result from the growth being more constrained by aridity than the carbon (C) gain, or reflect local adaptation to aridity, since NSC fuel metabolism and ensure adequate osmoregulation through the supply of SS, while low growth reduces water and C demands. It has been further proposed that C allocation to storage could come at the expense of growth (i.e., a growth–storage trade-off). We examined whether NSC and growth reflect the local adaptation to aridity in Embothrium coccineum J. R. Forst & G. Forst. (Proteaceae), a species with an exceptionally wide niche. To control for any influence of phenotypic plasticity on NSC and growth, we collected seeds from dry (46° 16′S, 71° 55′W, 500 mm year−1) and moist (45° 24′S, 72° 40′W, >2500 mm year−1) climates and grew seedlings in a common garden experiment for 3 years. We then compared the NSC and SS concentrations and pools (i.e., total contents) and the biomass of seedlings at spring, summer and fall. Seedlings from the dry climate had significantly lower biomass and similar NSC concentrations and pools as seedlings from moist climate, suggesting that reduced growth in arid environments does not result from a prioritization of C allocation to storage but that it confers advantages under aridity (e.g., lower transpiration area). Across organs, starch and NSC decreased similarly in seedlings from both climates from spring onward. However, root and stem SS concentrations increased during the growing season, and these increases were significantly higher in seedlings from the dry climate. The greater SS accumulation in seedlings from the dry climate compared with those from the moist climate demonstrates ecotypic differentiation in the seasonal dynamics of SS, suggesting that SS underlie local adaptation to aridity.