Ageing in trees: Role of body size optimization in demographic senescence

Abstract

“We must discover the reason why trees are of an enduring constitution” wrote Aristotle in 350 BCE. Millennial lifespans in clonal trees, reproductive activity in young and physically underdeveloped trees, and sustained (albeit sporadic) reproduction for life in most trees, have made others suggest that trees show negative (anti) senescence or even become immortal. Alternatively, we hypothesise that demographic senescence is always observed when trees reach their habitat-specific optimum body size. Natural selection optimizes body size in trees such that their age-specific mortality probability is minimized and fertility is maximised. Trees of supra-optimal size are vulnerable to extrinsic mortal threats. Size-driven decline in tree bodily function is accentuated by age-driven loss of access to genomic information through chromosomal reorganisation, epigenetic changes, and transcriptional inadequacies. Annual trends in fertility are unpredictable in trees, although fertility always declines in old trees because of age- and size-dependent functional decline and body mass loss. We propose that an increase in body size beyond a habitat-specific optimum will escalate size-specific mortality probability of trees without any significant gains in fertility. Such trees will show increasing mortality rate and decreasing fertility rate, a hallmark of demographic senescence. The time-course of demographic senescence is also influenced by the extent of juvenile mortality, age- and size-dependent changes in offspring quality, and heterogeneity in height growth rate. High juvenile mortality is the main reason why premature reproduction has evolved in trees of sub-optimal size. Offspring viability (a) remains poor in adults of sub-optimal size, (b) improves as these adults get bigger and attain an optimum size, and (c) may be sustained in older trees (with low fertility levels) due to a trade-off between fertility and seed viability, shaped by habitat-specific body size optimization. Senescence is not avoided, but slows down in (a) safe niches, where trees of supra-optimal body size survive, and in (b) extreme niches, where attainment of relatively shorter or smaller optimal size is protracted.