Bet‐hedging germination in annual plants: a sound empirical test of the theoretical foundations

Abstract

Seed dormancy is thought to be a key mechanism allowing annual plants to spread extinction risk in unpredictably varying environments. Theory predicts increasing germination fractions with increasing probability of reproductive success but solid empirical evidence is scarce and often confounded with environmental factors. Here we provide an empirical test of bet‐hedging via delayed germination for three annual plant species along a ‘predictability gradient’ in Israel. We excluded confounding environmental and maternal effects by raising inbred seed families and germinating them under controlled conditions. Additionally, we germinated field‐collected seeds in three consecutive seasons to compare their germination with inbred families where maternal effects were removed. Risk of reproductive failure was quantified using demographic data from the field and from second‐generation inbred lines raised in a rainfall gradient in the greenhouse. Our findings were consistent with bet‐hedging theory in that germination fraction was negatively related to species‐ and site‐specific risk of reproductive failure. Both field and hand‐raised seeds of one species exhibited higher dormancy with increasing risk of reproductive failure across sites, and hand‐raised seeds of another species showed the same pattern. The third species exhibited a rather random pattern of germination between years and sites, corresponding to the lack of site‐specific risk of reproductive failure. Species‐specific patterns of dormancy and risk could be related to alternative risk‐spreading strategies such as high adult survival, but were also affected by phylogeny. We provide strong empirical evidence for seed dormancy being a mechanism to reduce the risk of reproductive failure in highly variable environments, but a larger number of rigorous experimental tests of bet hedging germination are needed. Specifically, the genetic basis of bet‐hedging must be shown in species with different life histories, for demonstrating that dormancy is adaptive and how it is modified by other risk‐spreading traits.

Not only size matters: achene morphology affects time of seedling emergence in three heterocarpic species of <i>Anacyclus</i> (Anthemideae, Asteraceae)

“…This offers the chance to colonize new sites, free from sibling competition or other local sources of stress, whereas the remainder of the offspring stays in the same habitat (Gadgil, 1971;Levin & al., 1984;Schoen & Lloyd, 1984;Venable & Brown, 1993;Imbert & Ronce, 2001). Various authors have proposed that a bet-hedging strategy is likely to be favored in temporally variable environments because it increases geometric fitness, even if individual phenotypes may have a relatively lower mean fitness (Gillespie, 1977;Venable, 1985;Venable & al., 1987;Venable, 2007;Simons, 2011;Tielbörger & al., 2012).…”

“…This offers the chance to colonize new sites, free from sibling competition or other local sources of stress, whereas the remainder of the offspring stays in the same habitat (Gadgil, 1971;Levin & al., 1984;Schoen & Lloyd, 1984;Venable & Brown, 1993;Imbert & Ronce, 2001). Various authors have proposed that a bet-hedging strategy is likely to be favored in temporally variable environments because it increases geometric fitness, even if individual phenotypes may have a relatively lower mean fitness (Gillespie, 1977;Venable, 1985;Venable & al., 1987;Venable, 2007;Simons, 2011;Tielbörger & al., 2012).Among members of Asteraceae, the occurrence of heterocarpy is relatively high (Mandák, 1997;Imbert, 2002). Heterocarpic species in this family usually produce different achene morphs within the same capitulum (reviewed in Imbert, 2002), although exceptions in which achene variation occurs between aerial and subterranean capitula are known in Gymnarrhena micrantha (Koller & Roth, 1964) and Catananche lutea (Ruiz de Clavijo, 1995;Ruiz de Clavijo & Jiménez, 1998), and in Centaurea melitensis (Porras & Muñoz, 2000) between cleistogamous and chasmogamous capitula.…”

Fisher–Wright model with deterministic seed bank and selection

“…Dormancy and quiescence sometimes have surprising and counterintuitive consequences, similar to diffusion in activatorinhibitor models [21]. In the following study, we focus more specifically on the evolution of dormancy in plant species [13,24,39], but the theoretical models also apply to microorganisms and invertebrate species [10,33]. Seed banking is a specific life-history characteristic of most plant species, which produce seeds remaining in the soil for short to long periods of time (up to several generations), and it has large but yet underappreciated consequences [12] for the evolution and conservation of many plant species.…”

“…In effect, the model of [26] represents a special case, also called a weak seed bank, where the time for lineages to coalesce is finite because the maximum time that seeds can spend in the bank is bounded. In the following we mainly have the weak seed bank model in mind where the time in the seed bank is bounded to a small finite number assumed to be realistic for most plant species [13,24,38,39]. Even if we allow for unbounded times a seed may be stored within the soil, we assume that the germination probability decreases rapidly with age such that e.g.…”

“…In the present article, we propose a method to cover delays in population genetics caused by seedbanks. Dormancy of reproductive structures, that is seeds or eggs, is described as a bet-hedging strategy [9,12] in plants [13,24,39], invertebrates, e.g., Daphnia [10], and microorganisms [33] to buffer against environmental variability. Bet-hedging is widely defined as an evolutionary stable strategy in which adults release their offspring into several different environments, here specifically with dormancy at different generations in time, to maximize the chance of survival and reproductive success, thus magnifying the evolutionary effect of good years and dampening the effect of bad years [9,12].…”