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1. Seed banks alter the rate and direction of molecular evolution in Bacillus subtilis

   https://doi.org/10.1101/2021.10.05.463161  

   Shoemaker WR, Polezhaeva E (January 2021, bioRxiv)

   Fluctuations in the availability of resources constrains the growth and reproduction of individuals, which in turn effects the evolution of their respective populations. Many organisms are able to respond to 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. We find that the ability to enter a dormant state increases the accumulation of genetic diversity over time and alters the trajectory of mutations, findings that are recapitulated using simulations based on a simple mathematical model. While the ability to form a seed bank does not alter the degree of negative selection, we find that it consistently alters the direction of molecular evolution across genes. Together, these results show that the ability to form a seed bank affects 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. Molecular Evolutionary Dynamics of Energy Limited Microorganisms

   https://doi.org/10.1093/molbev/msab195  

   Shoemaker, William R; Polezhaeva, Evgeniya; Givens, Kenzie B; Lennon, Jay T (July 2021, Molecular Biology and Evolution)

   Battistuzzi, Fabia Ursula (Ed.)

   Abstract Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000 days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that although the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon. 

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4. Effect of the Seed Bank on Evolutionary Rescue in Small Populations: Univariate and Multivariate Demogenetic Dynamics

   https://doi.org/10.1086/731402  

   Godineau, Claire; Theodorou, Konstantinos; Spigler, Rachel B (September 2024, The American Naturalist)

   Under global change, the impact of seed banks on evolutionary rescue is uncertain. They buffer plant populations from demographic and genetic stochasticity but extend generation time and can become a reservoir of maladapted alleles. We built analytical and individual-based models to predict the effect of seed banks on the persistence of small annual plant populations facing an abrupt or sustained directional change in uni- or multivariate trait optima. Demogenetic dynamics predict that under most scenarios seed banks increase the lag yet enhance persistence to 200–250 years by absorbing demographic losses. Simulations indicate that the seed bank has a minimal impact on the genetic skew, although we suggest that this result could depend on the fitness component under selection. Our multivariate model reveals that by enlarging and reshaping the G matrix, seed banks can diminish the impact of mutational correlation and even accelerate adaptation under antagonistic pleiotropy relative to populations without a bank. We illustrate how the magnitude of optimum fluctuations, type and degree of optimum change, selection strength, and vital rates are weights that tip the scales determining persistence. Finally, our work highlights that migration from the past is not maladaptative when optimum fluctuations are large enough to create stepping stones to the new optimum. 

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5. 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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