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Fluctuating environments select for short-term phenotypic variation leading to long-term exploration.

ABSTRACT: Genetic spaces are often described in terms of fitness landscapes or genotype-to-phenotype maps, where each genetic sequence is associated with phenotypic properties and linked to other genotypes that are a single mutational step away. The positions close to a genotype make up its "mutational landscape" and, in aggregate, determine the short-term evolutionary potential of a population. Populations with wider ranges of phenotypes in their mutational neighborhood are known to be more evolvable. Likewise, those with fewer phenotypic changes available in their local neighborhoods are more mutationally robust. Here, we examine whether forces that change the distribution of phenotypes available by mutation profoundly alter subsequent evolutionary dynamics. We compare evolved populations of digital organisms that were subject to either static or cyclically-changing environments. For each of these, we examine diversity of the phenotypes that are produced through mutations in order to characterize the local genotype-phenotype map. We demonstrate that environmental change can push populations toward more evolvable mutational landscapes where many alternate phenotypes are available, though purely deleterious mutations remain suppressed. Further, we show that populations in environments with harsh changes switch phenotypes more readily than those in environments with more benign changes. We trace this effect to repeated population bottlenecks in the harsh environments, which result in shorter coalescence times and keep populations in regions of the mutational landscape where the phenotypic shifts in question are more likely to occur. Typically, static environments select solely for immediate optimization, at the expensive of long-term evolvability. In contrast, we show that with changing environments, short-term pressures to deal with immediate challenges can align with long-term pressures to explore a more productive portion of the mutational landscape.

SUBMITTER: Canino-Koning R

PROVIDER: S-EPMC6474582 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Project description:Climate change is increasingly exposing populations to rare and novel environmental conditions. Theory suggests that extreme conditions will expose cryptic phenotypes, with a concomitant increase in trait variation. Although some empirical support for this exists, it is also well established that physiological mechanisms (e.g. heat shock protein expression) change when organisms are exposed to constant versus fluctuating temperatures. To determine the effect of common, rare and novel temperatures on the release of hidden variation, we exposed fathead minnows, Pimephales promelas, to five fluctuating and four constant temperature regimes (constant treatments: 23.5, 25, 28.5 and 31°C; all fluctuating treatments shared a minimum temperature of 22°C at 00.00 and a maximum of 25, 28, 31, 34 or 37°C at 12.00). We measured each individual's length weekly over 60 days, critical thermal maximum (CTmax), five morphometric traits (eye anterior-posterior distance, pelvic fin length, pectoral fin length, pelvic fin ray count and pectoral fin ray count) and fluctuating asymmetry (FA, absolute difference between left and right morphometric measurements; FA is typically associated with stress). Length-at-age in both constant and fluctuating conditions decreased with temperature, and this trait's variance decreased with temperature under fluctuating conditions but increased and then decreased in constant temperatures. CTmax in both treatments increased with increasing water temperature, while its variance decreased in warmer waters. No consistent pattern in mean or variance was found across morphometric traits or FA. Our results suggest that, for fathead minnows, variance can decrease in important traits (e.g. length-at-age and CTmax) as the environment becomes more stressful, so it may be difficult to establish comprehensive rules for the effects of rarer or stressful environments on trait variation. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Project description:Increasing demand for river water now conflicts with an increasing desire to maintain riparian ecosystems. Efficiently managing river flows for riparian vegetation requires an understanding of the time scale of flow effects, but this information is limited by the absence of long-term studies of vegetation change in response to flow variation. To investigate the influence of short- and long-term flow variability and dam operation on riparian vegetation, we determined the occurrence of 107 plant species in 133 permanent plots of known inundating discharge along the Gunnison River in Colorado on five different occasions between 1990 and 2013. Individual species moved up and down the gradient of inundating discharge coincident with increases and decreases in mean annual flow, and the correlations between flow and species occurrence were strongest when flows were weighted by time before vegetation sampling with a median half-life of 1.5 years. Some tall, rhizomatous, perennial species, however, responded to flows on a longer time scale. Logistic regression of species occurrence showed a significant relation with inundation duration for 70 out of 107 species. Plot species richness and total vegetative cover decreased in association with desiccation at low inundation durations and with fluvial disturbance at high inundation durations. Within-plot similarity in species occurrence between years decreased strongly with increasing inundation duration. Moderate inundation durations were dominated by tall, rhizomatous, perennial herbs, including invasive Phalaris arundinacea (reed canary grass). Over the 23-year study period, species richness declined, and the proportion of rhizomatous perennials increased, consistent with the hypothesis that decreases in flow peaks and increases in low flows caused by flow regulation have decreased establishment opportunities for disturbance-dependent species. In summary, annual-scale changes in vegetation were strongly influenced by flow variation, and decadal-scale changes were influenced by decreases in fluvial disturbance from upstream flow regulation beginning decades prior to the onset of this study.

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Fluctuating environments select for short-term phenotypic variation leading to long-term exploration.

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