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

Abstract

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.

Keywords: Bet-hedging; Eco-physiology; Fitness; Heteromorphism; Seed dormancy; Soil seed bank.

Fig. 1

a Examples of plant anatomical parts showing bet-hedging strategies, b Example of caryopses heteromorphism in Poaceae: Aegilops geniculata Roth (photo and X-ray scan: F Guzzon)

Fig. 2

Trends of fitness in bet-hedging and specialization strategies in a stable and b unstable environments over time L = low; M = medium; H = high fitness. Dashed lines represent the geometric mean of fitness for each strategy. Comparisons are made between strategies, not environments

Fig. 3

Number of heteromorphic species and of species showing bet-hedging strategies distributed in different plant families as reported by Imbert (2002) and Scholl et al (2020), respectively.

Fig. 4

Network of processes related to bet-hedging