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Changing environments and genetic variation: natural variation in inbreeding does not compromise short-term physiological responses.

ABSTRACT: Selfing plant lineages are surprisingly widespread and successful in a broad range of environments, despite showing reduced genetic diversity, which is predicted to reduce their long-term evolutionary potential. However, appropriate short-term plastic responses to new environmental conditions might not require high levels of standing genetic variation. In this study, we tested whether mating system variation among populations, and associated changes in genetic variability, affected short-term responses to environmental challenges. We compared relative fitness and metabolome profiles of naturally outbreeding (genetically diverse) and inbreeding (genetically depauperate) populations of a perennial plant, Arabidopsis lyrata, under constant growth chamber conditions and an outdoor common garden environment outside its native range. We found no effect of inbreeding on survival, flowering phenology or short-term physiological responses. Specifically, naturally occurring inbreeding had no significant effects on the plasticity of metabolome profiles, using either multivariate approaches or analysis of variation in individual metabolites, with inbreeding populations showing similar physiological responses to outbreeding populations over time in both growing environments. We conclude that low genetic diversity in naturally inbred populations may not always compromise fitness or short-term physiological capacity to respond to environmental change, which could help to explain the global success of selfing mating strategies.

SUBMITTER: Buckley J

PROVIDER: S-EPMC6892046 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Changing environments and genetic variation: natural variation in inbreeding does not compromise short-term physiological responses.

Buckley James J Daly Rónán R Cobbold Christina A CA Burgess Karl K Mable Barbara K BK

Proceedings. Biological sciences 20191120 1915

Selfing plant lineages are surprisingly widespread and successful in a broad range of environments, despite showing reduced genetic diversity, which is predicted to reduce their long-term evolutionary potential. However, appropriate short-term plastic responses to new environmental conditions might not require high levels of standing genetic variation. In this study, we tested whether mating system variation among populations, and associated changes in genetic variability, affected short-term re ...[more]

PMID: 31744436

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Project description:Changing nutritional conditions challenge microbes and shape their evolutionary optimization. Here, we used real-time metabolomics to investigate the role of glycogen in the dynamic physiological adaptation of Escherichia coli to fluctuating nutrients following carbon starvation. After the depletion of environmental glucose, we found significant metabolic activity remaining, which was linked to rapid utilization of intracellular glycogen. Glycogen was depleted by 80% within minutes of glucose starvation and was similarly replenished within minutes of glucose availability. These fast time scales of glycogen utilization correspond to the short-term benefits that glycogen provided to cells undergoing various physiological transitions. Cells capable of utilizing glycogen exhibited shorter lag times than glycogen mutants when starved between periods of exposure to different carbon sources. The ability to utilize glycogen was also important for the transition between planktonic and biofilm lifestyles and enabled increased glucose uptake during pulses of limited glucose availability. While wild-type and mutant strains exhibited comparable growth rates in steady environments, mutants deficient in glycogen utilization grew more poorly in environments that fluctuated on minute scales between carbon availability and starvation. Taken together, these results highlight an underappreciated role of glycogen in rapidly providing carbon and energy in changing environments, thereby increasing survival and competition capabilities under fluctuating and nutrient-poor conditions.IMPORTANCE Nothing is constant in life, and microbes in particular have to adapt to frequent and rapid environmental changes. Here, we used real-time metabolomics and single-cell imaging to demonstrate that the internal storage polymer glycogen plays a crucial role in such dynamic adaptations. Glycogen is depleted within minutes of glucose starvation and similarly is replenished within minutes of glucose availability. Cells capable of utilizing glycogen exhibited shorter lag times than glycogen mutants when starved between periods of exposure to different carbon sources. While wild-type and mutant strains exhibited comparable growth rates in steady environments, mutants deficient in glycogen utilization grew more poorly in environments that fluctuated on minute scales between carbon availability and starvation. These results highlight an underappreciated role of glycogen in rapidly providing carbon and energy in changing environments, thereby increasing survival and competition capabilities under fluctuating and nutrient-poor conditions.

Project description:BACKGROUND AND AIMS:Since the early 1990s, research on genetic variation of phenotypic plasticity has expanded and empirical research has emphasized the role of the environment on the expression of inbreeding depression. An emerging question is how these two evolutionary ecology mechanisms interact in novel environments. Interest in this area has grown with the need to understand the establishment of populations in response to climate change, and to human-assisted transport to novel environments. METHODS:We compare performance in the field of outcrossed (O) and inbred lines (S1, S2) from 20 maternal families from each of two native populations of Mimulus guttatus. The experiment was planted in California in each population's home site, in the other populations's home site, in a novel site within the native range of M. guttatus, and in a novel site within the non-native range in North America. The experiment included nearly 6500 individuals. Survival, sexual reproduction and above-ground biomass were examined in order to evaluate inbreeding depression, and stem diameter and plant height were examined in order to evaluate phenotypic plasticity. KEY RESULTS:Across all field sites, approx. 36 % of plants survived to flowering. Inbreeding depression differed among sites and outcrossed offspring generally outperformed selfed offspring. However, in the native-novel site, self-progeny performed better or equally well as outcross progeny. Significant phenotypic plasticity and genetic variation in plasticity was detected in the two architectural traits measured. The absolute value of plasticity showed the most marked difference between home and non-native novel site or non-native-novel site. Evidence was detected for an interaction between inbreeding and plasticity for stem diameter. CONCLUSIONS:The results demonstrate that during initial population establishment, both inbreeding depression and phenotypic plasticity vary among field sites, and may be an important response to environments outside a species' currently occupied range. However, the interaction between inbreeding and plasticity may be limited and environment-dependent.

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Changing environments and genetic variation: natural variation in inbreeding does not compromise short-term physiological responses.

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Changing environments and genetic variation: natural variation in inbreeding does not compromise short-term physiological responses.

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