Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions

Abstract

Amphicarpy is a form of diversified bet-hedging expressed mostly in annual plants, where two types of offspring are produced with two distinct ecological roles: longrange aerial dispersers and highly competitive subterranean, sedentary fruit. Emex spinosa is a semi-arid, amphicarpic annual, inhabiting habitats with different levels of environmental variation. We tested the hypothesis that, in E. spinosa, bet-hedging may be ''finetuned'' by plasticity in the phenotype ratio (aerial/subterranean fruit mass) as a function of environmental conditions. We conducted a greenhouse experiment, manipulating nutrient availability and intraspecific density, to determine the pattern of ratio shifts. In order to determine whether the integrated strategy is an adaptation to variable habitats, a similar common garden experiment was conducted, comparing two natural populations differing in environmental variability. The offspring ratio shifted in response to both nutrient availability and plant density. In pots containing single plants the ratio increased steeply with nutrient availability, while in pots containing eight plants a more moderate increase occurred. These shifts were the result of plasticity in allocation to both achene types, as well as ontogenetic effects on aerial achene production. The degree of response increased with the heterogeneity of the habitat of origin. We found evidence for an adaptive integrated strategy, with bet-hedging ''fine-tuned'' by phenotypic plasticity. Strenuous conditions tended to shift the offspring ratio towards securing subterranean reproductive success, while favorable conditions resulted in a shift towards dispersible achenes.

Developmental Control and Plasticity of Fruit and Seed Dimorphism in Aethionema arabicum

“…Heteromorphism in plants has often been considered a mere bet-hedging strategy, emphasizing its independence from environmental conditions (Imbert, 2002). However, our data, in accordance with several other studies, demonstrate that, in some heteromorphic plant species, morph numbers and ratio show plasticity in response to certain environmental stimuli (Mandák and Pyšek, 1999;Imbert and Ronce, 2001;Sadeh et al, 2009;Lu et al, 2013b;Yang et al, 2015). Such a blend of bet hedging and plasticity should be expected to evolve when either the cue that predicts the future environment is weak or fitness is determined by predictable and unpredictable environmental factors alike (Bradford and Roff, 1993;Simons, 2011).…”

“…Several studies suggest that at least some heteromorphic species diminish this problem by means of phenotypic plasticity, defined as the ability of a genotype to produce different phenotypes when exposed to different environmental conditions (Via et al, 1995;Sultan, 2000;Pigliucci et al, 2006;Abley et al, 2016). The fruit-morph ratio of heteromorphic species may vary in response to herbivory (Imbert and Ronce, 2001), nutrient availability and plant density (Mandák and Pyšek, 1999;Sadeh et al, 2009;Lu et al, 2013a), germination time (Yang et al, 2015), and soil moisture (Lu et al, 2013a), indicating that these plants can adjust their fruit development in response to certain environmental parameters. However, so far, very little is known about the molecular determinants of heteromorphism in general and the plastic developmental modulation of this phenotype in particular.…”

A case for a joint strategy of diversified bet hedging and plasticity in the pea aphid wing polyphenism

“…These studies have focused mostly on dormancy emergence traits, such as seed germination timing in desert annuals [26] and diapause break in killifish [12]. Our study suggests that mixed strategies may also be common in dispersal traits, such as previously shown in an amphicarpic annual plant [27] and now in the pea aphid wing polyphenism.…”

Plasticity and within plant sex-ratio variation in monoecious Emex spinosa

“…This strategy is common in short-lived fugitive species whose habitat varies in time and space (Harper, 1977). Moreover, the bet-hedging strategy in amphicarpic plants can be "fine-tuned" by phenotypic plasticity (Sadeh et al, 2009). Organisms are also developmental systems that continually integrate internal and external signals to modulate gene expression (Sultan, 2004).…”

“…In this study we analyze flower production and sex ratio in response to light intensity of 2 populations of Emex spinosa (L.) Campd., a Mediterranean amphicarpic annual that occurs in habitats with different levels of environmental variation (Weiss, 1980;Ortiz et al, 2009;Sadeh et al, 2009). Architectural effects have been previously found to affect reproductive traits of Emex spinosa (Ortiz et al, 2009), and we postulate that architecture may also be affected by environmental conditions; in particular, we could expect a different degree of phenotypic plasticity at different architectural levels.…”