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Prior evolution in stochastic versus constant temperatures affects RNA virus evolvability at a thermal extreme.

ABSTRACT: It is unclear how historical adaptation versus maladaptation in a prior environment affects population evolvability in a novel habitat. Prior work showed that vesicular stomatitis virus (VSV) populations evolved at constant 37°C improved in cellular infection at both 29°C and 37°C; in contrast, those evolved under random changing temperatures between 29°C and 37°C failed to improve. Here, we tested whether prior evolution affected the rate of adaptation at the thermal-niche edge: 40°C. After 40 virus generations in the new environment, we observed that populations historically evolved at random temperatures showed greater adaptability. Deep sequencing revealed that most of the newly evolved mutations were de novo. Also, two novel evolved mutations in the VSV glycoprotein and replicase genes tended to co-occur in the populations previously evolved at constant 37°C, whereas this parallelism was not seen in populations with prior random temperature evolution. These results suggest that prior adaptation under constant versus random temperatures constrained the mutation landscape that could improve fitness in the novel 40°C environment, perhaps owing to differing epistatic effects of new mutations entering genetic architectures that earlier diverged. We concluded that RNA viruses maladapted to their previous environment could "leapfrog" over counterparts of higher fitness, to achieve faster adaptability in a novel environment.

SUBMITTER: Gloria-Soria A

PROVIDER: S-EPMC7319105 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Prior evolution in stochastic versus constant temperatures affects RNA virus evolvability at a thermal extreme.

Gloria-Soria Andrea A Mendiola Sandra Y SY Morley Valerie J VJ Alto Barry W BW Turner Paul E PE

Ecology and evolution 20200429 12

It is unclear how historical adaptation versus maladaptation in a prior environment affects population evolvability in a novel habitat. Prior work showed that vesicular stomatitis virus (VSV) populations evolved at constant 37°C improved in cellular infection at both 29°C and 37°C; in contrast, those evolved under random changing temperatures between 29°C and 37°C failed to improve. Here, we tested whether prior evolution affected the rate of adaptation at the thermal-niche edge: 40°C. After 40 ...[more]

PMID: 32607165

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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:Germination response to fluctuating temperatures is a mechanism by which seeds detect gaps in vegetation canopies and depth of burial in soil, and it is very important for plants. Thus, studies on the effect of fluctuating temperature on germination at the community level are valuable for understanding community structure and biodiversity maintenance. We determined the effects of two alternating temperatures (5/25°C and 10/20°C) and one constant temperature (15°C) on seed germination of 445 species in a grassland community on the eastern Tibet Plateau. Seed mass was determined for each species, and data on habitat, type of life cycle, altitudinal distribution and functional group (graminoids or forbs) were obtained from the literature. Taking all species into account, alternating temperatures increased germination percentages regardless of amplitude. Overall, species growing in disturbed ground showed a significant germination response to temperature fluctuation, but those living in Alpine/subalpine meadow, forest margin /scrub, marshland and dry sunny slope habitats did not. Species distributed only at high elevations (>2000m) did not show a significant germination response to temperature fluctuation, whereas those occurring at both high and low elevations had a significant positive response. Germination of annuals/biennials was significantly promoted by 5/25°C, but not by 10/20°C, whereas germination of perennials was significantly promoted by both 5/25°C and 10/20°C. Small-seeded species were more likely than large-seeded species to respond positively to fluctuating temperatures. Germination of forbs had a positive response to temperature fluctuation, but germination of graminoids did not. Regeneration ability by seeds for about 36% of the species studied in the grassland can be increased by temperature fluctuation. The differential response among species to alternating vs. constant temperatures helps maintain community structure and biodiversity. A positive germination response to temperature fluctuation can partly explain why there are more forbs in degraded meadows.

Dataset Information

Prior evolution in stochastic versus constant temperatures affects RNA virus evolvability at a thermal extreme.

Publications

Prior evolution in stochastic versus constant temperatures affects RNA virus evolvability at a thermal extreme.

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