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

Abstract

Reversible plasticity in phenotypic traits allows organisms to cope with environmental variation within lifetimes, but costs of plasticity may limit just how well the phenotype matches the environmental optimum.An additional adaptive advantage of plasticity might be to reduce fitness variance, or bet-hedging to maximize geometric (rather than simply arithmetic) mean fitness. Here we model the evolution of reaction norm slopes, with increasing costs as the slope or degree of plasticity increases. We find that greater investment in plasticity (i.e. steeper reaction norm slopes) is favoured in scenarios promoting bet-hedging as a response to multiplicative fitness accumulation (i.e. coarser environmental grains and fewer time steps prior to reproduction), because plasticity lowers fitness variance across environmental conditions. In contrast, in scenarios with finer environmental grain and many time steps prior to reproduction, bet-hedging plays less of a role and individual-level optimization favours evolution of shallower reaction norm slopes.We discuss contrasting predictions from this partitioning of the different adaptive causes of plasticity into short-term individual benefits versus long-term genotypic (bet-hedging) benefits under different costs of plasticity scenarios, thereby enhancing our understanding of the evolution of optimum levels of plasticity in examples from thermal physiology to advances in avian lay dates. Impact summaryPhenotypic plasticity is a key mechanism by which organisms cope with environmental change. Plasticity relies on the existence of some reliable environmental cue that allows organisms to infer current or future conditions, and adjust their traits in response to better match the environment. In contrast, when environmental fluctuations are unpredictable, bet-hedging favours lineages that persist by lowering their fitness variance, either among or within individuals. Plasticity and bet-hedging are therefore often considered to be alternative modes of adaptation to environmental change. However, we here make the point that plasticity also has the capacity to change an organism's variance in fitness across different environmental conditions, and could thus itself be part ofand not an alternative toa bet-hedging strategy.We show that bet-hedging at the genotype level affects the optimal degree of plasticity that individuals use to track environmental fluctuations, because despite a reduction in expected fitness at the individual level, costly investment in the ability to be plastic also lowers variance in fitness. We also discuss alternative predictions that arise from scenarios with different types of costs of plasticity. Evolutionary bet-hedging and phenotypic plasticity are both topics experiencing a renewed surge of interest as researchers seek to better integrate different adaptations to ongoing rapid environmental change in a range of areas of literature within ecology and evolution, including behavioural ecology, evolutionary physiology and life-history theory. We believe that...

Evolution of phenotypic plasticity during environmental fluctuations

“…Traditionally, conservative bet-hedging has thus been interpreted as a production of generalist phenotypes, suited for an average environment (Philippi & Seger, 1989). However, phenotypic plasticity should, in some cases, also be considered a type of conservative bethedging (Haaland et al ., 2021). This occurs when plasticity results in lower variance in fitness (due to the canalization of fitness) and, at the same time, lower expected arithmetic fitness but higher geometric mean fitness.…”

Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects

“…2012). Recently, the combination of phenotypic plasticity and bet-hedging has been theoretically investigated, suggesting that phenotypic plasticity could further minimize fitness variances caused by mismatches between phenotype and environment (Rádai 2020; Haaland et al . 2021).…”

“…We previously showed that the Parsley Frog successfully exploits two temporal niches in the Mediterranean region thanks to a high phenotypic plasticity of tadpole development to face very different seasonal environments (Jourdan-Pineau et al, 2012). Recently, the combination of phenotypic plasticity and bet-hedging has been theoretically investigated, suggesting that phenotypic plasticity could further minimize fitness variances caused by mismatches between phenotype and environment (Rádai, 2020; Haaland et al, 2021). Interestingly, in the wolf spider, temperature and day length leads to alternative developmental types within broods.…”

Looking to the past to understand the future: linking evolutionary modes of response with functional and life history traits in variable environments

“…For example, a fraction of seeds may germinate in response to good germination rains, but the remaining seeds stay dormant as a hedge against the risk that good germination rains may be followed by unfavorable conditions (Cohen, 1967; Gremer et al ., 2016). On the contrary, plasticity may itself be a bet‐hedging strategy if a genotype produces offspring with different levels of plasticity (Haaland et al ., 2021). Thus, we may see a combination of modes evolve and plants may be particularly effective at combining strategies.…”