Modes of response to environmental change and the elusive empirical evidence for bet hedging

Abstract

Uncertainty is a problem not only in human decision-making, but is a prevalent quality of natural environments and thus requires evolutionary response. Unpredictable natural selection is expected to result in the evolution of bet-hedging strategies, which are adaptations to long-term fluctuating selection. Despite a recent surge of interest in bet hedging, its study remains mired in conceptual and practical difficulties, compounded by confusion over what constitutes evidence for its existence. Here, I attempt to resolve misunderstandings about bet hedging and its relationship with other modes of response to environmental change, identify the challenges inherent to its study and assess the state of existing empirical evidence. The variety and distribution of plausible bet-hedging traits found across 16 phyla in over 100 studies suggest their ubiquity. Thus, bet hedging should be considered a specific mode of response to environmental change. However, the distribution of bet-hedging studies across evidence categoriesdefined according to potential strength-is heavily skewed towards weaker categories, underscoring the need for direct appraisals of the adaptive significance of putative bet-hedging traits in nature.

Phenotypic Diversity Using Bimodal and Unimodal Expression of Stress Response Proteins

“…When sensing the environment is too slow or too costly, populations can rely on genetic and phenotypic variation to balance survival and growth. For example, they may sacrifice growth in low stress conditions to increase fitness in other environments (1)(2)(3). In the past decade, bet hedging, a type of nongenetic variation between individuals, has gained attention for its role in multiple biological processes (1,3).…”

“…For example, they may sacrifice growth in low stress conditions to increase fitness in other environments (1)(2)(3). In the past decade, bet hedging, a type of nongenetic variation between individuals, has gained attention for its role in multiple biological processes (1,3). For instance, the presence of subpopulations of nongrowing persister cells allows bacterial populations to survive high concentrations of antibiotics that target cell growth (4).…”

Aberrant clones: Birth order generates life history diversity in Greater Duckweed, Spirodela polyrhiza

“…First, variation in turion phenology provides only a mechanism for diversification but cannot be interpreted as diversified bet hedging unless it is shown to increase long‐term fitness (Philippi & Seger, 1989). Tests of bet‐hedging theory are notoriously difficult to perform because fitness effects must be documented over multiple generations (Simons, 2011). In this instance, a test of optimal bet hedging would require an assessment of the fitness consequences of observed variance in phenology of turion formation over multiple seasons in which freeze‐up date of ponds is representative of variation over an evolutionarily relevant timescale.…”

“…Bet‐hedging traits evolve over the long term because they maximize geometric mean fitness despite reducing expected fitness over the shorter term (Dempster, 1955; Philippi & Seger, 1989; Seger & Brockmann, 1987). Bet hedging reduces intergenerational variance in fitness (Gillespie, 1974) and may occur either through diversification or through expression of conservative “safe” traits (Philippi & Seger, 1989; Seger & Brockmann, 1987; Simons, 2011). For example, organisms may diversify offspring phenotypes such as the timing of seed germination (Simons, 2009) if the fitness associated with timing cannot be predicted at the time the “decision” is made, ensuring that at least a fraction will succeed (Cohen, 1966; Seger & Brockmann, 1987).…”

“…Although our knowledge of the prevalence of bet‐hedging strategies is improving (Beaumont, Gallie, Kost, Ferguson, & Rainey, 2009; Graham, Smith, & Simons, 2014; Simons, 2011), our understanding of the mechanisms underlying the generation of diversification and of the joint expression of these two modes of response is underdeveloped.…”