The timescale of environmental fluctuations determines the competitive advantages of phenotypic plasticity and rapid evolution

Abstract

Organisms can respond to fluctuating environments by phenotypic plasticity and rapid evolution, both occurring on similar timescales to the environmental fluctuations. Because each adaptation mechanism has been independently studied, the effects of different adaptation mechanisms on ecological dynamics are not well understood. Here, using mathematical modeling, we compared the advantages of phenotypic plasticity and rapid evolution under conditions where the environment fluctuated between two states on various timescales. The results indicate that the advantages of phenotypic plasticity under environmental fluctuations on different timescales depend on the cost and the speed of plasticity. Both the speed of plastic adaptation and the cost of plasticity affect competition results, while the quantitative effects of them vary depending on the timescales. When the environment fluctuates on short timescales, the two populations with evolution and plasticity coexist, although the population with evolution is dominant. On moderate timescales, the two populations also coexist; however, the population with plasticity becomes dominant. On long timescales, whether the population with phenotypic plasticity or evolution is more advantageous depended on the cost of plasticity. Moreover, our results indicate that the mechanisms resulting in the dominance of the plastic population over the population with evolution are different depending on the timescales of environmental fluctuations. Therefore, the timescales of environmental fluctuations deserve more attention if we are to better understand the detailed competition results underlying phenotypic variation.

Specifying the timescale of early life unpredictability helps explain the development of internalising and externalising behaviours and their link with reproductive effort in adolescence

“…The relative importance of these processes is determined by a number of factors, including the timescale of variability (Berrigan & Scheiner, 2004). Variability that is too quick relative to the organisms capacity for developing a matching phenotype should not lead to significant predictive plasticity (Franch-Gras et al, 2017;Kasada & Yoshida, 2020;Kingsolver & Huey, 1998;Stomp et al, 2008). Such plasticity will be favoured when fluctuations in environmental conditions are frequent enough to pose an adaptive challenge but still infrequent enough so that developing a matching phenotype is possible.…”

Lack of response to pond desiccation by eggs and tadpoles of the Yungas Red-belly Toad (Melanophryniscus rubriventris) in an unpredictable environment

“…However, our results show that tadpoles of M. rubriventris do not respond to the reduction of water level by accelerating significantly the larval development. Developmental plasticity is favored when the conditions of the environment experienced by the developing organism are a good predictor of future environmental conditions and can thus serve as a cue for an appropriate phenotype (Kasada and Yoshida 2020). The cost of maintaining a plastic phenotype may outweigh the benefit of being able to respond appropriately to an unpredictable condition and should ensure that enough individuals survive to allow populations to evolve to altered environmental conditions (Amburgey et al 2016).…”

“…Natural selection favors resource allocation strategies that optimize this utilization over their life cycle and across varying ecological conditions (Ellis et al 2009). Most environments exhibit a gradient of climatic conditions (e.g., temperature, relative humidity, rainfall) or availability of resources (e.g., food or breeding sites), that D r a f t 3 imply temporal fluctuations in these conditions over short or long timescales (Kasada and Yoshida 2020). Within these timescales, variation can occur on a regular temporal scale, as with seasonal or diurnal patterns of environmental change, or on an irregular scale where favorable periods, of variable duration, are separated by unfavorable, and equally variable, periods (Kasada and Yoshida 2020).…”

“…Most environments exhibit a gradient of climatic conditions (e.g., temperature, relative humidity, rainfall) or availability of resources (e.g., food or breeding sites), that D r a f t 3 imply temporal fluctuations in these conditions over short or long timescales (Kasada and Yoshida 2020). Within these timescales, variation can occur on a regular temporal scale, as with seasonal or diurnal patterns of environmental change, or on an irregular scale where favorable periods, of variable duration, are separated by unfavorable, and equally variable, periods (Kasada and Yoshida 2020). In such unpredictable environments, the success of alternative strategies of life-history traits (i.e., those characteristics that determine rates of reproduction and associated patterns of development, growth, aging, and parental investment) is largely random (Song et al 2020).…”

Specifying the timescale of early life unpredictability helps explain the development of internalising and externalising behaviours

“…The relative importance of these processes is determined by a number of factors, including the timescale of variability 19 . Variability that is too quick relative to the organisms capacity for developing a matching phenotype should not lead to significant predictive plasticity 16 , 17 , 59 , 60 . Such plasticity will be favoured when fluctuations in environmental conditions are frequent enough to pose an adaptive challenge but still infrequent enough so that developing a matching phenotype is possible.…”