Bet-hedging across generations can affect the evolution of variance-sensitive strategies within generations

Abstract

In order to understand how organisms cope with ongoing changes in environmental variability it is important to consider all types of adaptations to environmental uncertainty on different time-scales. Conservative bet-hedging represents a long-term genotype-level strategy that maximizes lineage geometric mean fitness in stochastic environments by decreasing individual fitness variance, despite also lowering arithmetic mean fitness. Meanwhile, variance-prone (aka risk-prone) strategies produce greater variance in short-term payoffs because this increases expected arithmetic mean fitness if the relationship between payoffs and fitness is accelerating. Using two evolutionary simulation models, we investigate whether selection for such variance-prone strategies are counteracted by selection for bet-hedging that works to adaptively reduce fitness variance. We predict that variance-prone strategies will be favored in scenarios with more decision events per lifetime and when fitness accumulates additively rather than multiplicatively. In our model variance-proneness evolved in fine-grained environments (with lower correlations among individuals in energetic state and/or in payoffs when choosing the variable decision), and with larger numbers of independent decision events over which resources accumulate prior to selection. In contrast, geometric fitness accumulation caused by coarser environmental grain and fewer decision events prior to selection favors conservative bet-hedging via greater variance-aversion. We discuss examples of variance-sensitive strategies in optimal foraging, migration, life histories and cooperative breeding in light of these results concerning bet-hedging. By linking disparate fields of research studying adaptations to variable environments we should be more able to understand the effects in nature of human-induced rapid environmental change.

Individual reversible plasticity as a genotype‐level bet‐hedging strategy

“…When fitness accumulates multiplicatively, as occurs in coarse‐grained environments for traits that are expressed only once or a few times per lifetime, adaptive bet‐hedging at the genotype level (Haaland, Wright, & Ratikainen, 2019; Starrfelt & Kokko, 2012) can cause changes in the levels of individual investment in phenotypic plasticity. If plasticity costs are constantly expressed across environmental conditions, as is the case for maintenance costs, genetic costs and information acquisition costs ( sensu Auld et al., 2010; DeWitt et al., 1998), bet‐hedging favours a steeper reaction norm slope than that maximizing arithmetic mean fitness (Figures 1a and 2a).…”

“…Another factor modifying the extent to which a given trait is subject to selection for bet‐hedging is how often the trait is expressed within an individual's lifetime (see Haaland, Wright, & Ratikainen, 2019), and this is especially relevant in the case of reversible plasticity. If the trait is only expressed once per lifetime, fitness accumulation across distinct events only occurs among individuals.…”

“…For example, in coarse‐grained environments, traits relating directly to reproductive success (such as timing of reproduction) in semelparous annual or short‐lived organisms should maximize geometric mean fitness across all possible environmental conditions (since total failure in a very early/late year means the whole lineage goes extinct). Such traits should therefore be subject to evolution of adaptive bet‐hedging strategies (Haaland, Wright, & Ratikainen, 2019). On the other hand, traits expressed several times under a series of different environmental conditions within a lifetime can accumulate fitness additively across events.…”

Principles of seed banks and the emergence of complexity from dormancy

“…For example, in what is referred to as conservative bet-hedging, a plant might "always play it safe" by producing a smaller number of high-quality seeds, regardless of environmental conditions 28 . This generalist tactic increases the multiplicative growth rate (i.e., geometric mean fitness) of a lineage by decreasing its variance in performance over time 42 . An alternate strategy is diversified bet-hedging, which metaphorically is interpreted as "not putting all of your eggs in one basket".…”

Seasonality and competition select for variable germination behavior in perennials

“…Furthermore, longer lifespans with a larger number of selective events over which fitness can accumulate (e.g. an individual experiencing multiple consecutive breeding seasons with variable conditions) also reduces the need for any variance reduction if fitness payoffs among selective events are uncorrelated (Haaland et al 2019).…”