Ecological, (epi)genetic and physiological aspects of bet-hedging in angiosperms

Abstract

Key message Bet-hedging is a complex evolutionary strategy involving morphological, eco-physiological, (epi)genetic and population dynamics aspects. We review these aspects in flowering plants and propose further research needed for this topic. Bet-hedging is an evolutionary strategy that reduces the temporal variance in fitness at the expense of a lowered arithmetic mean fitness. It has evolved in organisms subjected to variable cues from the external environment, be they abiotic or biotic stresses such as irregular rainfall or predation. In flowering plants, bet-hedging is exhibited by hundreds of species and is mainly exerted by reproductive organs, in particular seeds but also embryos and fruits. The main example of bet-hedging in angiosperms is diaspore heteromorphism in which the same individual produces different seed/fruit morphs in terms of morphology, dormancy, eco-physiology and/or tolerance to biotic and abiotic stresses in order to ‘hedge its bets’ in unpredictable environments. The objective of this review is to provide a comprehensive overview of the ecological, genetic, epigenetic and physiological aspects involved in shaping bet-hedging strategies, and how these can affect population dynamics. We identify several open research questions about bet-hedging strategies in plants: 1) understanding ecological trade-offs among different traits; 2) producing more comprehensive phylogenetic analyses to understand the diffusion and evolutionary implications of this strategy; 3) clarifying epigenetic mechanisms related to bet-hedging and plant responses to environmental cues; and 4) applying multi-omics approaches to study bet-hedging at different levels of detail. Clarifying those aspects of bet-hedging will deepen our understanding of this fascinating evolutionary strategy.

Natural disturbances and masting: from mechanisms to fitness consequences

“…Filling these pools and persisting until disturbances trigger reproduction, however, comes at a cost: reducing the temporal variance of fitness is traded against a lower (arithmetic) mean fitness. Under uncertainty of reproductive success, such bet-hedging strategies spread the risks over time and maximize the geometric mean fitness (but reduce the arithmetic mean fitness) [16,[121][122][123][124]. Bet-hedging strategies occur in hundreds of species [16,123,124].…”

“…Under uncertainty of reproductive success, such bet-hedging strategies spread the risks over time and maximize the geometric mean fitness (but reduce the arithmetic mean fitness) [16,[121][122][123][124]. Bet-hedging strategies occur in hundreds of species [16,123,124]. By analysing a global seed bank database of over 2300 angiosperm species, Gioria et al [125] found that higher rates of disturbances increased the likelihood of persistent seed banks, thus corroborating the evolutionary relevance of storing reproductive potential in habitats with low disturbance predictability.…”

Functional packaging of seeds

“…In different populations of the candlestick banksia ( Banksia attenuata ), plants develop follicles (responsive systems) with different valve curvatures along a climatic gradient, which results in higher levels of serotiny and higher opening temperatures in drier regions (Huss et al ., 2018). These morphological adaptations and the corresponding differences in physical dormancy and serotiny are often interpreted as bet‐hedging strategies to maximize survival in unpredictable environments (Clarke et al ., 2013; Arshad et al ., 2018; Yang et al ., 2020; Gianella et al ., 2021). In bet‐hedging species, dormancy appears to be linked to a higher polyphenol content in seed coats, resulting in darker morphs (Gianella et al ., 2021).…”

“…These morphological adaptations and the corresponding differences in physical dormancy and serotiny are often interpreted as bet‐hedging strategies to maximize survival in unpredictable environments (Clarke et al ., 2013; Arshad et al ., 2018; Yang et al ., 2020; Gianella et al ., 2021). In bet‐hedging species, dormancy appears to be linked to a higher polyphenol content in seed coats, resulting in darker morphs (Gianella et al ., 2021). In the barrelclover Medicago truncatula (Fabaceae), four genes related to the flavonoid metabolism and seven peroxidases and thio/peroxiredoxins have been associated with differential dormancy along an aridity gradient (Renzi et al ., 2020).…”

“…(2008)), storage periods before, during, or after dispersal, and germination. Particularly in regions with irregular rainfall, the seed stage often involves diaspore heteromorphism (Arshad et al ., 2018; Yang et al ., 2020; Gianella et al ., 2021), environmentally regulated dispersal (e.g. Seale & Nakayama, 2020), and extended storage periods in the canopy (termed serotiny; Lamont et al ., 2020) or in the soil (known as dormancy; Baskin & Baskin, 2014).…”