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1. Seed banks alter the molecular evolutionary dynamics of Bacillus subtilis

   https://doi.org/10.1093/genetics/iyac071  

   Shoemaker, William R.; Polezhaeva, Evgeniya; Givens, Kenzie B.; Lennon, Jay T.; Tellier, ed., A. (May 2022, Genetics)

   Abstract Fluctuations in the availability of resources constrain the growth and reproduction of individuals, which subsequently affects the evolution of their respective populations. Many organisms contend with such fluctuations by entering a reversible state of reduced metabolic activity, a phenomenon known as dormancy. This pool of dormant individuals (i.e. a seed bank) does not reproduce and is expected to act as an evolutionary buffer, though it is difficult to observe this effect directly over an extended evolutionary timescale. Through genetic manipulation, we analyze the molecular evolutionary dynamics of Bacillus subtilis populations in the presence and absence of a seed bank over 700 days. The ability of these bacteria to enter a dormant state increased the accumulation of genetic diversity over time and altered the trajectory of mutations, findings that were recapitulated using simulations based on a mathematical model of evolutionary dynamics. While the ability to form a seed bank did not alter the degree of negative selection, we found that it consistently altered the direction of molecular evolution across genes. Together, these results show that the ability to form a seed bank can affect the direction and rate of molecular evolution over an extended evolutionary timescale. 

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2. Bacteria-phage coevolution with a seed bank

   https://doi.org/10.1038/s41396-023-01449-2  

   Schwartz, Daniel A.; Shoemaker, William R.; Măgălie, Andreea; Weitz, Joshua S.; Lennon, Jay T. (June 2023, The ISME Journal)

   Abstract Dormancy is an adaptation to living in fluctuating environments. It allows individuals to enter a reversible state of reduced metabolic activity when challenged by unfavorable conditions. Dormancy can also influence species interactions by providing organisms with a refuge from predators and parasites. Here we test the hypothesis that, by generating a seed bank of protected individuals, dormancy can modify the patterns and processes of antagonistic coevolution. We conducted a factorially designed experiment where we passaged a bacterial host (Bacillus subtilis) and its phage (SPO1) in the presence versus absence of a seed bank consisting of dormant endospores. Owing in part to the inability of phages to attach to spores, seed banks stabilized population dynamics and resulted in minimum host densities that were 30-fold higher compared to bacteria that were unable to engage in dormancy. By supplying a refuge to phage-sensitive strains, we show that seed banks retained phenotypic diversity that was otherwise lost to selection. Dormancy also stored genetic diversity. After characterizing allelic variation with pooled population sequencing, we found that seed banks retained twice as many host genes with mutations, whether phages were present or not. Based on mutational trajectories over the course of the experiment, we demonstrate that seed banks can dampen bacteria-phage coevolution. Not only does dormancy create structure and memory that buffers populations against environmental fluctuations, it also modifies species interactions in ways that can feed back onto the eco-evolutionary dynamics of microbial communities. 

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3. Adaptive Phenotypic Plasticity Stabilizes Evolution in Fluctuating Environments

   https://doi.org/10.3389/fevo.2021.715381  

   Lalejini, Alexander; Ferguson, Austin J.; Grant, Nkrumah A.; Ofria, Charles (August 2021, Frontiers in Ecology and Evolution)

   Fluctuating environmental conditions are ubiquitous in natural systems, and populations have evolved various strategies to cope with such fluctuations. The particular mechanisms that evolve profoundly influence subsequent evolutionary dynamics. One such mechanism is phenotypic plasticity, which is the ability of a single genotype to produce alternate phenotypes in an environmentally dependent context. Here, we use digital organisms (self-replicating computer programs) to investigate how adaptive phenotypic plasticity alters evolutionary dynamics and influences evolutionary outcomes in cyclically changing environments. Specifically, we examined the evolutionary histories of both plastic populations and non-plastic populations to ask: (1) Does adaptive plasticity promote or constrain evolutionary change? (2) Are plastic populations better able to evolve and then maintain novel traits? And (3), how does adaptive plasticity affect the potential for maladaptive alleles to accumulate in evolving genomes? We find that populations with adaptive phenotypic plasticity undergo less evolutionary change than non-plastic populations, which must rely on genetic variation from de novo mutations to continuously readapt to environmental fluctuations. Indeed, the non-plastic populations undergo more frequent selective sweeps and accumulate many more genetic changes. We find that the repeated selective sweeps in non-plastic populations drive the loss of beneficial traits and accumulation of maladaptive alleles, whereas phenotypic plasticity can stabilize populations against environmental fluctuations. This stabilization allows plastic populations to more easily retain novel adaptive traits than their non-plastic counterparts. In general, the evolution of adaptive phenotypic plasticity shifted evolutionary dynamics to be more similar to that of populations evolving in a static environment than to non-plastic populations evolving in an identical fluctuating environment. All natural environments subject populations to some form of change; our findings suggest that the stabilizing effect of phenotypic plasticity plays an important role in subsequent adaptive evolution. 

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4. A century of genetic variation inferred from a persistent soil‐stored seed bank

   https://doi.org/10.1111/eva.12675  

   Summers, Jennifer L.; Bernik, Brittany; Saunders, Colin J.; McLachlan, Jason S.; Blum, Michael J. (July 2018, Evolutionary Applications)

   Abstract Stratigraphic accretion of dormant propagules in soil can result in natural archives useful for studying ecological and evolutionary responses to environmental change. Few attempts have been made, however, to use soil‐stored seed banks as natural archives, in part because of concerns over nonrandom attrition and mixed stratification. Here, we examine the persistent seed bank ofSchoenoplectus americanus, a foundational brackish marsh sedge, to determine whether it can serve as a resource for reconstructing historical records of demographic and population genetic variation. After assembling profiles of the seed bank from radionuclide‐dated soil cores, we germinated seeds to “resurrect” cohorts spanning the 20th century. Using microsatellite markers, we assessed genetic diversity and differentiation among depth cohorts, drawing comparisons to extant plants at the study site and in nearby and more distant marshes. We found that seed density peaked at intermediate soil depths. We also detected genotypic differences among cohorts as well as between cohorts and extant plants. Genetic diversity did not decline with depth, indicating that the observed pattern of differentiation is not due to attrition. Patterns of differentiation within and among extant marshes also suggest that local populations persist as aggregates of small clones, likely reflecting repeated seedling recruitment and low immigration from admixed regional gene pools. These findings indicate that persistent and stratified soil‐stored seed banks merit further consideration as resources for reconstructing decadal‐ to century‐long records that can lend insight into the tempo and nature of ecological and evolutionary processes that shape populations over time. 

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5. Rapid evolution during climate change: demographic and genetic constraints on adaptation to severe drought

   https://doi.org/10.1098/rspb.2023.0336  

   Benning, John W.; Faulkner, Alexai; Moeller, David A. (May 2023, Proceedings of the Royal Society B: Biological Sciences)

   Populations often vary in their evolutionary responses to a shared environmental perturbation. A key hurdle in building more predictive models of rapid evolution is understanding this variation—why do some populations and traits evolve while others do not? We combined long-term demographic and environmental data, estimates of quantitative genetic variance components, a resurrection experiment and individual-based evolutionary simulations to gain mechanistic insights into contrasting evolutionary responses to a severe multi-year drought. We examined five traits in two populations of a native California plant, Clarkia xantiana , at three time points over 7 years. Earlier flowering phenology evolved in only one of the two populations, though both populations experienced similar drought severity and demographic declines and were estimated to have considerable additive genetic variance for flowering phenology. Pairing demographic and experimental data with evolutionary simulations suggested that while seed banks in both populations likely constrained evolutionary responses, a stronger seed bank in the non-evolving population resulted in evolutionary stasis. Gene flow through time via germ banks may be an important, underappreciated control on rapid evolution in response to extreme environmental perturbations. 

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